Effect of Cd on Gene Expression in Plants: History
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Contributor:
Dagmar Moravčíková
,
Jana Žiarovská

Cadmium (Cd) is a heavy metal that can cause damage to living organisms at different levels. Even at low concentrations, Cd can be toxic to plants, causing harm at multiple levels.Previous studies have shown that Cd negatively affects the regulation of energy metabolism genetics pathways, genetics hormone pathways, enzymatic genetics pathways, and phytohormone biosynthesis. These ultimately interfere with the expression of genes in response to Cd-induced stress.

  • Cadmium
  • hyperaccumulators
  • genes

1. ATP-Binding Cassette Transporter Gene Family

Plants employ ATP-binding cassette transporters, or ABC transporters, to carry out various functions. One of these functions involves upholding homeostasis when the plant is exposed to heavy metals [1]. The most critical processes that have evolved in plants to protect them from negative effects such as Cd are the glutathione—dependent phytochelatin, as has been mentioned and PDR8-dependent pathways [2]. AtPDR8 is one of the fifteen genes encoding the family of ABC transporters in Arabidopsis thaliana, showing overall altered regulation following exposure to external and internal stressors [3]. WRKY13 has a unique role in response to exposure of Cd. Moreover, their upregulation increases resilience to stress from Cd. They affect upregulation of PDR8 in Arabidopsis thaliana, which decreases accumulation Cd in plants [4]. Plants with overexpression of MMDH2 have been detected in the regulation of the PDR8 gene in a negative way [5]. The fact that higher expression of the PDR8 gene helps plants become more resilient was described. Moreover, it has been concluded that AtPDR8 acts as a pump for draining excess Cd in Arabidopsis thaliana [6].

2. PCR Gene Family

To date, PCRs have not been sufficiently well studied. However, it has been shown to be able to transfer Cd and zinc (Zn) in plants. They contain the CCXXXXCPC and CLXXXXCPC motifs and also the PLAC8 motif. How much, if at all, these motifs are related to Cd and Zn transfer is not yet known [7]. Several regulated genes from this family of genes have been discovered in a variety of plants. HvPCR2 plays an important role in the detoxification of Hordeum vulgare L. [8]. SaPCR2 gene is regulated in Sedum alfredii [9]. The OsPCR1 gene has been found to be associated with detoxification and accumulation [10]. Subsequently, another gene was discovered in Oryza sativa [11]. The results were obtained using two different plant species, so that the focus was on the difference in their ability to accumulate Cd. Overexpression of the gene SIPCR6 underpinned the high resistance of Salix linearistipularis. Its function was verified using the established transgenic Populus [12].

3. ZIP Gene Family

Homologous genes occurring in the plant kingdom may not show the same expression after exposure to Cd. Evidence shows that expression of homologues ZIP family genes in Oryza sativa after Cd treatment is different than in Arabidopsis thaliana. The difference is in the location of expression. While in Arabidopsis thaliana, there is a higher expression of ZIP genes, especially in the root, in Oryza sativa, it is mostly in the shoot. Interestingly, quite the opposite regulation of specific genes: AtIRT3, AtZIP5, AtZIP12, OsIRT1 and OsZIP1 was detected [13]. An increase in the expression of the OsIRT1 and OsIRT2 genes has been observed in response to Fe deficiency. This overexpression, according to one study, could lead to increased uptake of Cd into the plant. The author goes on to explain that, thanks to OsIRT1, cadmium does not enter the plant through the roots, but is subsequently transported to other parts of the plant as well [14]. AtZIP9 and AtIRT1 genes were further detected, where expression was decreased in the roots of Arabidopsis thaliana. If a disturbance of expression in AtFC1 occurs, there is a change in gene transcription.. Detoxification processes in plants with high Cd exposure comprise mainly genes that are involved in GSH-dependent phytochelatin synthetic pathway [15]. A link has been found between WRKY33 and the expression of ATL31, which subsequently affects expression of the IRT1 gene. The whole mechanism works on the principle of decreasing absorption of Cd. After Cd treatment, gene encodes WRKY33 is upregulated. In theory, it links to the promotor of the ATL31 gene. ATL31 causes degradation of IRT1. Although the IRT1 transporter is the primary carrier for iron, it is also involved in transporting of other metals, including Cd [16]. It is likely that the transfer of a particular metal depends on a conserved residue in or in the immediate vicinity of the transmembrane domain [17]. Cd displaces other elements, such as Fe, Zn and Mn, from the transport pathways [18].

4. CDF/MTP Gene Family

The CDF gene family is also named MTPs, which means metal tolerance proteins. In Citrus sinensis L. overexpression of eight genes was detected in CitMTP1, CitMTP3, CitMTP4, CitMTP5, CitMTP7, CitMTP10, CitMTP11, and CitMTP12 in the underground section of plant. Apart from in the leaves overexpression of five genes was detected in CitMTP1, CitMTP3, CitMTP5, CitMTP8, and CitMTP12. Samples used in the research was affected by Cd for 7 days and 15 days with the form of Cd 0.038 mM CdSO4 and 0.38 mM CdSO4. The highest expression was analysed in CitMTP11 gene in the root with 0.038 mM CdSO4 and 15 days affected by Cd [19]. Increases in PCR gene expression were also detected in the sensitive plant Glycine max. In the leaves were upregulated genes GmaMTP1.1, GmaMTP1.2, GmaMTP3.1, GmaMTP3.2 and GmaMTP4, whereas in root were upregulated GmaMTP1.1, GmaMTP1.2, GmaMTP3.1, GmaMTP4.1, GmaMTP4.3, GmaMTP10.4, and GmaMTP11.1 [20]. In Fagopyrum tartaricum one gene FtMTP8.2 has been detected so far [21]. In Medicago truncatula there are twelve known CDS genes, of which five respond to Cd. MtMTP1.2 and MtMTP4 are upregulated in the root, MtMTP1.2 and MtMTP4 in stems, MtMTP4 in leaves. Based on bioinformatics analyses, it grouped all of the MTP genes in Medicago truncatula into clusters, and within these clusters, the genes showed a high degree of concordance. Further analyses showed that these genes contain domains that can be influenced by abiotic stressors and hormones [22].

5. NRAMP Gene Family

Many NRAMP genes have been identified in plants so far. These NRAMP genes are famous for encoding metal transporters. The study of plant genomes using modern techniques has led to new insights into the adaptive processes that have played an important role during evolution [23]. Phylogenetic studies show that the number of introns and motif in the NRAMP genes family is changing. This information could mean that plants are adapting to stresses during evolution. A consequence of NRAMP genes being able to respond to heavy metals-induced stress is that the promoters of these genes contain many motifs or elements. In a comparative study, the MYB MYC and STRE elements were the most abundant in the observed Spirodela polyrhiza plant. In addition, ABRE motifs linked with the hormones were present in the compared plants. Following Cd exposure, the expression of NRAMP genes in the plant is altered. The genes SpNramp1, SpNramp2, and SpNramp3 of Spirodela polyrhiza are sensitive to Cd treatment. These genes showed their activity mainly in the root [24]. In Arabidopsis thaliana, NRAMP genes AtNRAMP2, AtNRAMP3, AtNRAMP4 and AtNRAMP5 contain up to 67–75% conserved regions in amino acid sequence. After Cd treatment overexpression, the AtNRAMP3 gene causes changes in Fe accumulations and root growth [25]. That this gene is involved in the maintenance of metal homeostasis is also demonstrated by Oomen [26]. Furthermore, the function of these genes in response to heavy metals was analysed in Thlaspi caerulescens. Expression of NRAMP3 and NRAMP4 was significantly higher in Thlaspi caerulescens than in Arabidopsis thaliana [26]. It has been discovered that there is a difference in gene expression, specifically NRAMP1, NRAMP2, NRAMP3, NRAMP5 and NRAMP6 in two varieties of peppers [27]. OsNRAMP1 has also been discovered in Oryza sativa which is associated with increased uptake and accumulation in the plant [28].

6. ACS and ACO Multigene Family

It is established that ACO and ACS share a common role in the production of ethylene [29] and that the overexpression of their genes by Cd leads to an increase in the production of ethylene. The further determined genes which are involved in response to heavy metals have been demonstrated in previous studies. An increase of gene expression of ACS1, ACS2, ACS4, ACS5, ACS6, ACS7, ACS8 was identified in Arabidopsis thaliana after Cd treatment. While the higher level of the expression in the root was ACS6 after 72 h, in the leaves was after 24 h. These studies have also observed increased expression in members of the ACO multigene family. The most highly expressed genes, ACO2 and ACO4 were detected in the roots and in leaves after Cd treatment [30].

7. HIPP/HPP Gene Family

The number of genes encoding HIPP/HPP in plants is very high. In some plant species, there are more than two hundred [31]. The OsHIPP56 gene is thought to play an important role. For testing this, the CRISPR/Cas9 technique was used to create rice in which this gene was knocked out. The mutation resulted in large amounts of Cd entering the edible parts of the plant [32].

8. PCs Gene Family

The PCS1 and PCS2 genes have also been implicated in the response to Cd in plants defence mechanisms. However, the transcriptomic level is also influenced by ZAT6, which belongs to the ZIP transporter family [33]. Strikingly, in the study by Santoro [34] in the plant Arundo donax L., Cd did not alter the expression of PCS genes. This is a consequence of the fact that in this experiment, the plant defence mechanism was not triggered by PCS [34]. Following the application of 50 μM Cd in Vicia sativa, the VsPC1 gene was upregulated, probably leading to increased tolerance to Cd [35]. It is suggested that PCS1 is affected by overexpression of the MAN3 gene. MAN3 in Arabidopsis thaliana is important in responding to heavy metal stress. After exposure to Cd, there is an increase in the expression of MAN3. MAN3 has a critical role in increasing mannose concentration and the consequent activation of PC synthesis related genes such as PCS1 and PCS2 [36]. This whole cascade likely contains up to four different components involved in responding to Cd. This entire complex includes the MYB4 transcription factor, which binds to the MAN3 gene and the MAN3-mediated mannose-binding-lectin 1 (MNB1) gene. It is the MNB1-related GNA domain that influences the resistance of this complex, as it is capable of association with MAN3 [37].

9. MT Gene Family

MTs provide sites on their genes for transcription factors to bind, resulting in differential expression and response to heavy metal exposure. A differential expression of the ZmMTs has been found in Zea mays. In the underground part of the plant, the expression of ZmMT3 and ZmMT7 genes is reduced. On the one hand, a higher expression of ZmMT3, and lower expression of ZmMT1, ZmMT7 and ZmMT8 were observed in the stems. In the leaves, a different expression was observed. The ZmMT3, ZmMT7 and ZmMT9 genes were more highly expressed and the ZmMT1 and ZmMT8 genes were less highly expressed [38]. Additional studies identified the Spirodela polyrhiza SpMT2a gene, which is highly likely to be involved with Cd tolerance based on expression at the transcriptome level after 24 h [39]. The genes MTB2, MTB3 and MTB15 were found to be upregulated in Calotropis gigantea L. [40]. In Oryza sativa and Triticum aestivum, there is a relatively high probability that HsfA4a influences the MT genes, and thus enhances the defence of the plants [41].

10. Antioxidant Genes

The presence of SOD genes in plants enhances their ability to withstand stress caused by different abiotic factors [42]. The presence or expression of antioxidant enzymes such as SOD can enhance the plant’s ability to resist damage caused by Cd exposure. However, the expression of genes related to antioxidant enzymes such as POD, CAT, APX, FeSOD, and MnSOD varies with the concentration of Cd present. Interestingly, these genes do not exhibit similar expression patterns and respond differently to varying levels of Cd. These observations have been validated in the case of Lolium perenne L. [43]. Following Cd treatment in Lolium perenne L., overexpression of SOD genes was observed. These genes encode different isoforms of SOD, including Cyt Cu/ZnSOD, MnSOD, and ChlCu/ZnSOD, each with unique expression patterns. The maximum expression of Cyt Cu/Zn SOD gene is between 6–24 h, while the maximum expression of MnSOD is between 4–6 h and the overexpression of MnSOD is also between 4–6 h [44]. In another plant, many SOD genes have been studied that are essential for the response to Cd treatment. Kandelia obovata was also examined for the expression of a family of SOD genes. A recent study has provided insight into the KoCSD1, KoCSD2, KoCSD3, KoFSD1, KoFSD2, KoFSD3 and KoMSD genes and their expression after exposure to Cd. By means of the quantitative RT-PCR method, they conclude that each of these genes is upregulated after Cd treatment. There was a significant upregulation in the roots and in the above-ground parts of Kandelia obovata. There has been an interesting breakthrough about gene expression in medical plants [45]. Two years later, selected KoFSD2 and KoCSD3 genes were published and transferred into Nicotiana bethamiana, where they came up with the idea that it was KoCSD3 that might have a function in plant defence, preventing Cd from reaching the roots by affecting the roots at the cellular level. Its overexpression in the root exodermis confirmed this discovery [46]. Gene BjCAT3 from Brassica juncea was studied in connection with Cd exposure. The changes of expression were observed by the Northern block. To confirm the association of this gene with Cd, a transgenic plant was generated where higher expression of this gene was shown to be associated with Cd [5].

11. HMA Gene Family

HMA genes, particularly HMA1 and HMA2, were overexpressed in another study [27]. Several genes in plants such as NcHMA4 and NcHMA3 in Noccaea caerulescens, AhHMA3 Arabidopsis halleri in shoots [47], SpHMA7 [48] and SpHMA3 in Sedum plumbizincicola [49], OsHMA3 in Oryza sativa [50] were reported. A detailed analysis of all eight HMA-encoding genes was performed for Sedum plumbizincicola. This led to the conclusion that these genes contain the elements DKTGT, GDGxNDxP, PxxK S/TGE, HP and CPx/SPC [48]. Twenty-one genes encoding HMA have been identified in Hordeum vulgare L., Hv. From this number, five HMA genes were selected that had changes in regulation by Cd [51]. Analyses comparing HMA-encoding genes in Arabidopsis thaliana and Brassica rapa var. rapa showed that the genes in Brassica rapa var. rapa had undergone evolutionary changes. The genes have been separated into two groups. Different heavy metals species are associated with each group. Out of a total of fourteen genes, upregulation changes were observed for four genes BrrHMA1, BrrHMA2.1, BrrHMA2.2 and BrrHMA4.1, which were observed in roots of Cd-resistant plants. The upregulation of the BrrHMA2.2 gene in the root was observed in the Cd-sensitive variety, while over expression of the other genes was not observed here. One gene, BrrHMA1, showed the opposite expression in the sensitive plant, where it was downregulated, and conversely upregulated in the resistant plant [52]. Table 1 is a summary of the genes that were affected by Cd treatment. The genes are divided into groups called families. These are shown in the first column. The second column is the plant in which the gene was under regulation and the third column is the gene identification number from the NCBI database [53]. The fourth column gives the name of the gene and the fifth column gives the gene’s function in relation to Cd treatment.
Table 1. Genes regulated by Cd treatment.
Gene Family Plant Gene ID Gene Function Reference
ABC Arabidopsis thaliana BK001007.1 AtPDR8 Cd transport [6]
Oryza sativa 4327728 ABCG36 Cd transport [1]
ACS Arabidopsis thaliana 825324 ACS1 Cd tolerance [30]
Arabidopsis thaliana 837082 ACS2 Cd tolerance [30]
Arabidopsis thaliana 816812 ACS4 Cd tolerance [30]
Arabidopsis thaliana 836709 ACS5 Cd tolerance [30]
Arabidopsis thaliana 826730 ACS6 Cd tolerance [30]
Arabidopsis thaliana 828726 ACS7 Cd tolerance [30]
Arabidopsis thaliana 829933 ACS8 Cd tolerance [30]
Antioxidant genes Lolium perenne L. N/A MnSOD Cd tolerance [43]
Kandelia obovata N/A KoFSD2 Cd tolerance [46]
Kandelia obovata N/A KoCSD3 Cd tolerance [46]
CDF/MTP Citrus sinensis L. N/A CitMTP1 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP3 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP4 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP5 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP7 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP10 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP11 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP12 Cd tolerance [19]
Citrus sinensis L. N/A CitMTP8 Cd tolerance [19]
Glycine max N/A GmaMTP1.1 Cd tolerance [20]
Glycine max N/A GmaMTP1.2 Cd tolerance [20]
Glycine max N/A GmaMTP3.1 Cd tolerance [20]
Glycine max N/A GmaMTP3.2 Cd tolerance [20]
Glycine max N/A GmaMTP4 Cd tolerance [20]
Glycine max N/A GmaMTP4.3 Cd tolerance [20]
Glycine max N/A GmaMTP10.4 Cd tolerance [20]
Glycine max N/A GmaMTP11.1 Cd tolerance [20]
Fagopyrum tartaricum N/A FtMTP8.2 Cd tolerance [21]
Medicago truncatula N/A MtMTP1.2 Cd tolerance [22]
Medicago truncatula N/A MtMTP4 Cd tolerance [22]
Medicago truncatula N/A MtMTP1.2 Cd tolerance [22]
Medicago truncatula N/A MtMTP4 Cd tolerance [22]
HMA Oryza sativa 4342783 OsHMA3 Cd translocation, acccumulation [54]
MT Sedum plumbizincicola MK893990.1 SpMT2 Cd detoxification [55]
Zea mays N/A ZmMT3 Cd tolerance [38]
Zea mays N/A ZmMT7 Cd tolerance [38]
Zea mays N/A ZmMT1 Cd tolerance [38]
Zea mays N/A ZmMT7 Cd tolerance [38]
Zea mays N/A ZmMT8 Cd tolerance [38]
Spirodela polyrhiza N/A SpMT2a Cd tolerance [39]
Calotropis gigantea N/A MTB2 Cd tolerance [40]
Calotropis gigantea N/A MTB3 Cd tolerance [40]
Calotropis gigantea N/A MTB15 Cd tolerance [40]
NRAMP Arabidopsis thaliana 841127 AtNRAMP2 Cd transport [25]
Arabidopsis thaliana 816847 AtNRAMP3 Cd transport [25]
Arabidopsis thaliana 836868 AtNRAMP4 Cd transport [25]
Arabidopsis thaliana 827613 AtNRAMP5 Cd transport [25]
Arabidopsis thaliana 838166 AtNRAMP6 Cd transport [56]
Glycine max 100812381 NRAMP2A Cd transport [57]
Glycine max 100815628 NRAMP5A Cd transport [57]
Glycine max 100789871 NRAMP1B Cd transport [57]
Glycine max 100791117 NRAMP3A Cd transport [57]
Glycine max 100797298 NRAMP6A Cd transport [57]
Oryza sativa 4342862 OsNRAMP1 Cd transport [28]
Spirodela polyrhiza N/A SpNramp1 Cd transport [24]
Spirodela polyrhiza N/A SpNramp2 Cd transport [24]
Spirodela polyrhiza N/A SpNramp3 Cd transport [24]
Capsicum annuum N/A NRAMP1 Cd transport [27]
Capsicum annuum N/A NRAMP2 Cd transport [27]
Capsicum annuum N/A NRAMP3 Cd transport [27]
Capsicum annuum N/A NRAMP5 Cd transport [27]
Capsicum annuum N/A NRAMP6 Cd transport [27]
PCR Oryza sativa N/A OsPCR1 Cd detoxification [10]
Salix linearistipulari N/A SlPCR6 Cd detoxification [12]
Hordeum vulgare L. N/A HvPCR2 Cd detoxification [8]
Sedum alfredii N/A SaPCR2 Cd detoxification [9]
PCs Arabidopsis thaliana 831845 PCS1 Cd detoxification [33]
Arabidopsis thaliana 839354 PCS2 Cd detoxification [33][58]
Arabidopsis thaliana 828409 GSH1 Cd tolerance [59]
Arabidopsis thaliana 832797 GSH2 Cd tolerance [59]
Arabidopsis thaliana 842387 AtIRT3 Cd transport [13]
ZIP Arabidopsis thaliana 836336 AtZIP12 Cd transport [13]
Arabidopsis thaliana N/A AtZIP5 Cd transport [13]
Arabidopsis thaliana 829439 AtZIP9 Cd transport [15]
Arabidopsis thaliana 827713 AtIRT1 Cd transport [15]
Arabidopsis thaliana 820457 AtZIP1 Cd transport [15]
Oryza sativa 4333669 OsIRT1 Cd transport [14][60]
Oryza sativa 4333667 OsIRT2 Cd transport [14]
Oryza sativa AY324148.1 OsZIP1 Cd transport [13]
Energetic pathway Oryza sativa 4342404 LOC4342404 Unknown [61]
Oryza sativa 4347395 LOC4347395 Unknown [61]
Oryza sativa 4334300 LOC4334300 Unknown [61]
Oryza sativa 4352085 LOC4352085 Unknown [61]
Oryza sativa 4335799 LOC4335799 Unknown [61]
Oryza sativa 4342192 OS07G0105600 Unknown [61]
Oryza sativa 4329766 LOC4329766 Unknown [61]
Oryza sativa 4344281 LOC4344281 Unknown [61]
Oryza sativa 4347336 LOC4347336 Unknown [61]
Oryza sativa 4344281 LOC4344281 Unknown [61]
Signalling pathway Oryza sativa 4347336 LOC4347336 Unknown [61]
Oryza sativa 4324556 LOC4324556 Unknown [61]
Oryza sativa 4332175 OS03G0235000 Unknown [61]
Oryza sativa 4332175 LOC4332175 Unknown [61]
Peroxidase pathway Oryza sativa 4337483 LOC4337483 Unknown [61]
Oryza sativa 4337892 LOC4337892 Unknown [61]
Oryza sativa 4350051 LOC4350051 Unknown [61]
Oryza sativa 4349585 LOC4349585 Unknown [61]
Oryza sativa 4324556 LOC4324556 Unknown [61]
Oryza sativa 4332175 OS03G0235000 Unknown [61]
Oryza sativa 4332175 LOC4332175 Unknown [61]
Oryza sativa 4337483 LOC4337483 Unknown [61]
Oryza sativa 4337892 LOC4337892 Unknown [61]
Oryza sativa 4350051 LOC4350051 Unknown [61]
Oryza sativa 4349585 LOC4349585 Unknown [61]

This entry is adapted from the peer-reviewed paper 10.3390/plants12091848

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