Molecular Breeding to Develop HMT Tolerance in Rice

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This entry is adapted from the peer-reviewed paper 10.3390/agriculture13050944

Heavy metal toxicity generally refers to the negative impact on the environment, humans, and other living organisms caused by exposure to heavy metals (HMs). Heavy metal poisoning is the accumulation of HMs in the soft tissues of organisms in a toxic amount. HMs bind to certain cells and prevent organs from functioning. Agricultural experts have expressed interest in further investigating the underlying mechanisms that allow plants to resist HM toxicity. Given a thorough understanding of HM transport and deposition in various plant organelles, researchers have proposed a number of experimental methods using innovative molecular approaches that can assist rice plants develop HM tolerance. In particular, detoxification, transport, and/or sequestration are the primary objectives of HM control techniques. Fluid transport from roots to other plant parts involves water transpiration, root pressure, cation exchange in the cell walls of xylem vessels, formation of complexes with amino acids (Cu), histidine, peptides (Ni), and chelates with organic acids (Zn). Accordingly, the concentrations of most HMs gradually decreased with distance from the root. These elements are transported inside the plant by cell wall charge interactions and the formation of soluble organic complexes in the sap.

rice heavy metals stress tolerance molecular breeding

1. Role of HM Transporters (HMTs) and Tolerant Proteins (HMPs)

Previously reported P1B subfamily of HM transporters P-type ATPases (HMAs) affect HM uptake and transport in different plants ^[1]^[2]^[3]. The researchers found upregulation of HMA genes and retrotransposons in rice after HM treatment and intergenerational inheritance of altered expressions ^[4]. This study demonstrated how rice plants respond to HM stress by altering locus-specific gene expression and trans-generational inheritance due to altered gene regulation, even after HM stress has been eliminated. Fu et al. linked a G-type ATP-binding cassette transporter OsABCG36 to Cd tolerance in rice. Cd-induced OsABCG36 was expressed localized to the plasma membrane in protoplast cells of the root tip and mature roots. Knockdown of OsABCG36 increased Cd accumulation in roots and enhanced sensitivity to Cd stress without affecting tolerance to other HMs (i.e., Al, Zn, Cu, and Pb) ^[5].

Metal tolerance proteins (MTPs), another type of membrane protein, have also been demonstrated to be involved in metal transport and to impart tolerance to certain HMs in plants. In a comprehensive molecular study of rice MTP genes, three thousand rice genotypes were investigated using available genome-wide resequencing information, highlighting the evolution and allelic diversity of MTP genes ^[6]. These findings indicated that MTP1, MTP8.1 and MTP9, MTP11 localize to QTL/m-QTL for Zn and Cd accumulation, respectively. MTP9 and MTP8.1 had specific root and shoot expression, respectively, at all stages of the rice plants. After getting exposed to toxic HMs, it was determined that some seed-specific MTPs regulated metal transport during the seed-filling stage downregulated the expression of the majority of MTP genes in the roots, and upregulated those in the shoots, indicating that MTP employs various mechanisms in different tissues.

Certain HM-associated proteins (HMPs) have been reported to be involved in HM detoxification. In earlier studies, the novel genes were found to regulate a protein known as cell number regulatory factor (CNR) in plants e.g., TaCNR2 in wheat and ZmCNR1 in maize ^[7]. This protein, like the cadmium-tolerant protein in plants, modulates cell number and HM transport. Overexpression of TaCNR2 in rice also increases stress resistance to Cd, Zn, and Mn, and their translocation from roots to shoots. TaCNR2 has been shown through experimental studies to transport HM ions, providing another source of genes that improve nutrient absorption and decrease the buildup of hazardous metals in rice plants ^[8]. Li et al. also identified 46 HMPs in rice, which they named OsHMPs 1–46 according to their chromosomal locations. Studies have shown that HMPs are governed by different TFs, and only 8 OsHMPs are assembled in rice tissues. Among them, OsHMP37 had a much higher expression level than the other seven HMPs, whereas OsHMP28 was solely expressed in the roots. Only OsHMP09, OsHMP18, and OsHMP22 showed increased expression levels in all tissues, despite the fact that most of the selected OsHMPs were variably expressed in different tissues under varying HM exposures ^[9]. Approximately 43 putative Fe–S cluster assembly genes have also been identified in the rice (Oryza sativa) genome and the expression of all genes has been validated ^[10]^[11]. Liang et al. investigated the role of Fe–S cluster assembly in leaf chloroplasts are particularly sensitive to HM treatment, and genes encoding Fe–S cluster assembly in roots are sensitive to iron toxicity, oxidative stress, and HM stress; and are shown to be upregulated in response ^[11]. OsHMA2 is a major Zn/Cd transporter identified in rice roots and has been experimentally shown to promote Zn/Cd transfer from roots to shoots. ^[12].

2. Role of microRNAs (miRNAs)

In several investigations, high-throughput sequencing and miRNA microarray data have indicated the involvement of several miRNAs in the responses of various plant species to toxic HMs ^[13]. Overexpression of miRNAs or the development of miRNA-resistant target genes have been widely utilized to demonstrate the role of metal-responsive miRNAs, and these miRNAs and their target genes are an essential component of a large-scale regulatory network controlling different metabolic processes in response to metal stress ^[14]^[15]. Several regulatory networks involving miRNAs and their TFs have been studied ^[16]. Ding et al., identified twelve (12) Cd-responsive miRNAs in rice using miRNA microarray assays. Expression of another Cd-responsive miRNA (miR166) was significantly suppressed under Cd exposure at the seedling stage and its overexpression reduced Cd-induced oxidative stress ^[17]. Overexpression of miR166 also reduced root-to-shoot Cd translocation and Cd accumulation in rice grains ^[12]^[18].

3. QTL and Fine Gene Mapping

Researchers have extensively used genetic markers in rice crops to identify genomic loci involved in various plant physiological functions under simulated stress conditions and associated tolerance mechanisms ^[19]^[20]. Breeders have used the same approach to identify QTLs associated with specific HM accumulation, translocation, and tolerance strategies in rice to reduce HM toxicity ^[21]. Arsenic is the most toxic of all HM and rice absorbs more arsenic than other crops ^[22]. Once the crop has absorbed HM through its roots, it is distributed throughout the plant and then transferred to the rice grain ^[23]. The International Agency for Research on Cancer (IARC) declared As, Cd, and Cr to be highly carcinogenic and can damage DNA by disrupting DNA synthesis/repair mechanisms and resulting in neuropsychiatric disorders ^[24]. Due to climate change, more arsenic is expected to be present in the environment as more rain releases arsenic and other HM previously trapped in mining areas ^[25]. Ingestion of 1 mg of arsenic per day can affect the skin for several years ^[26]. Therefore, As has now become the most priority research area among plant breeders. Numerous QTL mapping and genome-wide association studies (GWAS) have documented a number of QTLs/candidate genes that confer toxicity tolerance and HM accumulation in rice (Oryza sativa L.) ^[27]. In an investigation, an early backcross population from a cross between WTR1 (indica) and Haoannon (japonica) was grown hydroponically and exposed to As (10 ppm) for seven days and genotyped using 704 SNP markers. One QTL for relative chlorophyll content was identified on chromosome 1, two QTLs for arsenic content in roots were discovered on chromosome 8, and six QTLs for arsenic content in shoots were identified on chromosomes 2, 5, 6, and 9 ^[28].

Tyagi et al. ^[29] found that the tolerant genotypes accumulated less Al and showed a minimal reduction in root-shoot biomass under Al stress compared to susceptible genotypes. Transcriptomic data indicated that tolerant genotypes conserved energy by down-regulating key glycolytic pathway genes in roots, maintaining transcription levels of key energy-releasing enzymes, up-regulated signaling, and regulatory transcripts encoding zinc finger proteins and cell wall-associated transcripts under Al stress. Stein et al. ^[30] also designed a similar study to identify candidate genes for iron toxicity tolerance by investigating the effect of excess iron on two rice cultivars with apparent tolerance to iron toxicity. These results suggest that physiological and anatomical changes and HM permeability in various parts of rice may be related to toxic tolerance.

Shilin et al. ^[31] also investigated the genetic mechanism of Cd tolerance in rice, using a RIL population derived from crossing two parents (i.e., PA64s and 93–11) to analyze the associated QTLs to cadmium tolerance at the seedling stage. Two QTLs, i.e., qCDSL1.1 and qCDSL1.2 were identified in Hangzhou and Lingshui, respectively. The Chromosomal Segment Replacement Line, CSSLqCDSL1 was developed in the context of parent 93–11 which contained qCDSL1.1/qCDSL1 from parent PA64. Under Cd stress conditions, CSSLqCDSL1 had a longer shoot length compared to 93–11, demonstrating tolerance to Cd toxicity. In another investigation by Maghrebi et al. ^[32] two major rice cultivars (i.e., Capataz and Beirao) with different Cd tolerance were exposed to various Cd concentrations (0.01, 0.1, and 1 μM) and their potential capacities to sequester and transfer Cd. QTL mapping for toxic metal/metalloid stress tolerance in rice identified three QTLs associated with As, one associated with Cu and Hg, and two associated with Fe and Zn content.

In a genome-wide association study (GWAS), 188 different cultivated rice germplasms were examined at the seedling stage under normal and Cd stress conditions. By combining GWAS data, transcriptome analysis, database gene annotation intelligent Gene Ontology (GO), and homologous gene annotation and function, 148 candidate Cd-mediated growth response (CGR) genes were obtained ^[33]. In another GWA study, the correlation between arsenic and eight essential ions in the rice germplasm population was analyzed and it was shown that the association between arsenic and other essential ions was affected by growing conditions and various genetic factors. A cis-eQTL for AIR2 (arsenic-induced RING finger protein) was isolated by transcriptome-wide association studies, and the expression level of AIR2 was confirmed to be lower in indica than in japonica. By genome-wide analysis, arsenic-associated QTLs were discovered on chromosomes 5 and 6 under submerged and intermittent submerged conditions ^[22].

Another GWA study on low Cd accumulation in rice identified the OsABCB24 gene as the basis of a new QTL (qCd1-3) ^[34]. GWAS of trace iron and zinc in rice grains revealed novel associations of marker traits with 2.1–53.0% phenotypic variation, which may help identify candidate genes for increased iron tolerance and zinc ^[35]. Fe toxicity in rice crops was also investigated using a GWAS approach, and three linkage disequilibrium (LD) blocks were found to contribute primarily to Fe omission on chromosomes 1, 2, 3, 4, and 7 ^[36]. Other GWA studies found 22, 17, and 21 QTLs in rice associated with As, Cd, and Pb toxicity, respectively. To identify genomic areas regulating the covariance between mineral elements in the rice genome, Liu et al. used multivariate QTL analysis and principal component analysis (PCA). They sequenced the entire genome of rice RILs and identified potential candidate loci under the QTL clusters, including OsHMA4 and OsNRAMP5 ^[37].

4. HM Tolerant Transgenic Rice

Over the past decade, genetically modified (GM) crops have been officially adopted in many countries around the world, with their coverage increasing rapidly every year. Therefore, extensive research has been conducted on genetically modified (GM) rice in particular, focusing on the development of rice species tolerant to various biotic and abiotic factors ^[38]. Researchers are now also focusing on developing genetically modified rice by inserting new genes, which could reduce the buildup of HM in rice grains ^[39]^[40]. For instance, glutathione peroxidase (PgGPx) was discovered to impart salt and drought resistance to transgenic rice plants in a previous investigation ^[39]. The peroxidase gene family plays an essential role in maintaining ion homeostasis because it transports metal ions, including Cd ^[41]^[42]. Elaborated the role of PgGPx on Cd stress in rice and found that PgGPx transcript level was strongly up-regulated in response to exogenous Cd level. Under Cd stress, overexpression of PgGPx in transgenic rice improves control of ROS scavenging pathways and cellular ion homeostasis maintenance.

Another multigene family of plant-specific peroxidases (Class III) is involved in various physiological and developmental processes and tolerates abiotic stresses and HM such as aluminum, zinc, cadmium, and copper by removing ROS and RNS ^[43]. In a study, Kidwai et al. ^[44] identified a class III peroxidase (OsPRX38) from rice that was consistently increased in response to arsenate (As) and arsenite stress. Overexpression of OsPRX38 in transgenic rice significantly increased arsenic (As) tolerance by regulating lignin biosynthesis which acts as an apoplast barrier for As entry into root cells, resulting in reduced As accumulation in transgenics. Another protein (MTH1745) from the thermophilic archaea Methanothermobacter thermoautotrophicum has already been shown to prevent citrate synthase aggregation after heat denaturation and to play an important role in heat stress resistance ^[16]. Overexpression of MTH1745 in transgenic rice plants also increased mercury tolerance and increased photosynthesis rate compared to non-transgenic rice. Chen et al. ^[45] & Ding et al. ^[46] down-regulated the expression of miR5144-3p and overexpressed OsPDIL1-1, respectively, in transgenic rice plants which significantly improved mercury stress tolerance.

Researchers improved rice varieties low in As, Cd, and Cs by eliminating the genes (such as OsNRAMP5, OsNRAMP1, OsARM1, and OsHAK1) ^[47]^[48]. Other transporters such as OsNRAMP1 have been identified as a mediator of Cd and Mn uptake ^[49]. Overexpression of another gene, LmMTP1, metal resistance protein 1 (MTP1), isolated from ryegrass, resulted in increased resistance to Zn, Co, and Cd in transgenic lines ^[50]. Overexpression of microRNA (miR166) enhanced tolerance to Cd toxicity in transgenic rice plants thereby reducing Cd accumulation in grains ^[17]. Plants overexpressing OsHB4 have been shown to have increased sensitivity to cadmium and accumulate cadmium in their leaves. Conversely, OsHB4 silencing increased the tolerance of transgenic plants to Cd.

In a study, to limit arsenic in the roots of rice plants as a detoxification mechanism, the phytochelatin synthase CdPCS1 from cornflower, an arsenic-accumulating aquatic plant, was transgenically expressed ^[40]. Increased arsenic accumulation in roots and shoots was observed in transgenic rice lines. However, compared to non-transgenic plants, all transgenic lines accumulated much less arsenic in grain and hulls. Huang et al. ^[51] identified OsHMA4 in yeast as a possible causative gene of a QTL controlling Cu accumulation in rice grains and provided evidence that OsHMA4 functions as a Cu chelate in root vacuoles, limiting the accumulation of Cu in grains. The resulting transgenic lines were more resistant to HM stress than the nontransgenic or wild type.

Gu et al. isolated DEFENSIN 8 (DEF8), a defensin-like gene expressed in rice grains, and suggested that DEF8 promotes Cd loading into the xylem and mediates Cd translocation from root to shoot and subsequent distribution in the grain ^[52]. DEF8 is also a modulator of Cd unloading to the phloem without affecting the accumulation of essential mineral nutrients and key crop traits ^[53]. Li ^[9] reported that low cadmium accumulation rice lines could be constructed by overexpressing a truncated OsO3L2 gene. Researchers have successfully developed rice plants that reduce cadmium accumulation by overexpressing the rice genes OsO3L2, OsO3L3, or their truncated versions ^[13]. Since the tissue localization of both these genes showed high expression in roots, it seems possible that roots are involved in low Cd accumulation. According to another study, transgenic rice plants overexpressing V-PPase accumulated more cadmium in the roots than in the shoots ^[54]. Similarly, another mutant line overexpressing the OsHIPP16 (OE) gene significantly improved rice growth under Cd toxicity stress ^[55].

5. CRISPR/Cas Genome Editing

In the past decade, advanced genome engineering technology, CRISPR-Cas9 has also been used to improve detoxification efficiency in rice by targeting HM-specific genes ^[56]^[57] (Table 1). Gene function and the way in which it affects other biochemical processes are changed by indel mutations and targeted substitutions generated through the CRISPR/Cas9 system. The OsNRAMP1 gene that controls the uptake of various HMs (including Cd, Fe, As, and Mn) in various crops was successfully deleted by the gene editing approach, which also greatly reduced the uptake and storage of Cd and As in the grains of rice ^[58]. Cd accumulation in rice was studied by deleting a segment of the OsABCG36 gene by CRISPR/Cas9 technology. Cd tolerance developed in knockout mutants as a result of Cd accumulation in root cells and excretion of the Cd content from the cytosol to detoxify its effects ^[5]. The OsLsi gene family has been reported to be involved in Si xylem loading in rice roots, which is required for efficient Si transport from roots to stems. CRISPR-Cas-based inactivation of this gene (OsLsi) resulted in reduced Si uptake in xylem sap and also reduced As accumulation in rice ^[59]. Similarly, CRISPR/Cas9 has been used to knock down OsNramp5 and OsLCT1 to reduce cadmium (Cd) accumulation ^[60] and inactivate the low cesium (Cs) K+ transporter OsHAK1 in rice plants ^[48]. Overexpression of gene OsLCT2 (a low-affinity cation transporter) using CRISPR-Cas9 also reduced Cd accumulating in rice grains ^[61]. More recently other genome-editing technologies, such as CRISPR-Cas12a, CRISPR-directed evolution, and base-editors, have also succeeded in more efficiently multiplex genome-editing in rice ^[11].

Table 1. List of targeted genes modified for HM tolerance in rice using CRISPR-Cas9 genome editing technology.

Metalloid	Targeted Gene(s)	Molecular Functions	Role in HM Toxicity Tolerance	References
As, Si	OsLsi	Silicon (Si) transporter	Low arsenic uptake	^[59]
Cd	OsABCG36	G-type ATP-binding cassette (ABC) transporter	Cadmium sequestration and toxicity tolerance	^[5]
Cs	OsHAK1	High-Affinity Potassium (K+) Transporter	Low cesium accumulation in root and shoots	^[48]
As, Cd	OsNRAMP1	Cadmium, Iron, and manganese uptake/transporter	Low arsenic and cadmium content in grains	^[58]
Cd, Pb, Mn, Fe	OsNRAMP5	Major transporter for metal uptake	Low cadmium content in grains	^[60]
Cd	OsLCT1	Low-Affinity Cation Transporter	Low cadmium uptake	^[60]
Cd	OsLCT2	Low-Affinity Cation Transporter	Low cadmium accumulation in grains	^[61]

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Zulqarnain Haider

Irshan Ahmad

Samta Zia

Yinbo Gan

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Update Date: 16 May 2023

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