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Rice (
Rice (
Arsenic is ubiquitous in the environment and its contamination in soil and water has been reported in many countries. In aerobic soils, As is mainly present in the oxidized form as arsenate (AsV). While in anaerobic environments like paddy soil, it mainly exists in the reduced form as arsenite (AsIII) (
Arsenic exposure through drinking water adversely impacts millions of people, leading to increased cancer risk (
The As in rice grain is present primarily as inorganic AsIII and AsV, with a considerable proportion (typically 20–50%) of organic As, mainly as dimethylarsinic acid (DMAV) (
Research has uncovered the physiology of how plants deal with As. While arsenic accumulation in rice can be reduced by modifying cultural practices (
Critical gene families and representative genes from different species involved in As uptake, transport and metabolism.
Gene category | Gene name | Source | Manipulation | Consequence | Reference |
---|---|---|---|---|---|
Phosphate transporter (AsV transport) | Knockout | Increased AsV tolerance | |||
Knockout | Decreased AsV uptake; Increased AsV tolerance | ||||
Aquaporins (AsIII transport) | Knockout | Decreased As accumulation in straw of field-grown rice | |||
Knockout | Increased AsIII tolerance; Decreased As accumulation | ||||
Knockout | Increased shoot As tolerance; Decreased shoot As | ||||
Overexpression ( |
AsIII sensitivity; Increased As accumulation | ||||
Arsenate reductase | Knockout or overexpression | No effect on As accumulation | |||
Knockout | AsV sensitivity; Decreased As efflux from roots; Increased As accumulation in the shoots | ||||
Overexpression (rice) | Increased AsIII efflux into the external medium; Decrease As accumulation in rice grain | ||||
Glutaredoxin | Overexpression ( |
Increased As tolerance; Decreased As in leaves | |||
Overexpression ( |
Increased As tolerance; Decreased As accumulation | ||||
Phytochelatin synthase | Overexpression (rice) | Decreased As accumulation in grain | |||
NRAMP transporter (Fe/Mn/Cd/As transport) | Overexpression (rice) | Increased As tolerance and accumulation | |||
ABC transporter (Cd/Pb/As transport) | Overexpression ( |
Increased As tolerance and accumulation | |||
Overexpression ( |
Increased As tolerance | ||||
Overexpression ( |
Increased As tolerance | ||||
ACR3 transporter (AsIII efflux) | Overexpression (rice) | Increased As efflux; Decreased As in grain | |||
Overexpression ( |
Increased As efflux; Decreased As accumulation under AsIII in short-term exposure; Increased shoot As accumulation in soil in long-term cultivation | ||||
ArsB/NhaD permease (AsIII efflux) | Knockout | As sensitivity and As accumulation | |||
Knockout | Decreased As accumulation | ||||
ArsM/AS3MT family (As methylation) | Overexpression (rice) | Produced methylated volatile arsenic | |||
Expression ( |
Conferred resistance to AsIII | ||||
Overexpression ( |
As methylation to DMAV and As sensitivity | ||||
Inositol transporters (As transport) | Knockout | Lower shoot As accumulation | |||
CRT-like transporter (Glutathione homeostasis) | Knockout | Lower As accumulation in roots but higher or similar As accumulation in shoots | |||
Arsenate is the main As species in aerobic soils but it accounts for a small amount of total As in flooded paddy soils (
Arsenite, a neutral molecule, is the dominant As species in flooded paddy soils (
Besides Lsi1 (OsNIP2;1), other NIPs including OsNIP1;1, OsNIP2;2, OsNIP3;1, and OsNIP3;2 also show permeability to AsIII (
In contrast to the AsIII transporters, Fe plaque plays a role in sequestrating As and reducing As uptake by rice (
A number of methylated As species have been detected in soils, among them, monomethylarsonic acid (MMAV) and DMAV are the most common (
Arsenite has high affinity to sulfhydryl (–SH) groups of peptide thiol such as glutathione (GSH) and phytochelatins (PCs), thus AsIII is detoxified by complexing with GSH or PCs in plants (
In yeast, besides AsIII extrusion, there is a second pathway for As detoxification, i.e., vacuolar sequestration of AsIII by YCF1 (Yeast Cadmium Factor) (
Rice nodes are important hubs for controlling its elemental distribution (
A study on As unloading into rice grain shows that DMAV is translocated to the rice grain with over 10 times greater efficiency than inorganic species and is more mobile than AsIII in both phloem and xylem transport (
A simple method to decrease As in rice is to select cultivars that biologically restrict As accumulation in the grains as some rice cultivars accumulate 20–30 fold less As than others (
Former studies showed that ACR2 arsenate reductase, like AtACR2 in
In
In addition, the glutaredoxin may also play a role in AsV reduction and regulating the cellular AsIII levels, though the mechanistic details for its function are yet to be resolved (
Plants can rapidly reduce AsV to AsIII in the roots, which could then be effluxed out into external medium (
In yeast, AsIII is extruded into the external environment by the AsIII efflux transporter ACR3 (Arsenic Compounds Resistance protein 3) (
As-hyperaccumulator
The fact that an ACR3 from
After introducing yeast
In plants, AsIII-PC can be sequestrated into vacuoles as a step of As detoxification in cells, which also affects As allocation in plant tissues. In rice, OsABCC1 mediates vacuolar AsIII–PC sequestration, thus reducing As accumulation in rice grains (
Overexpressing transporters for As sequestration in the shoots may lead to As accumulation in plants (
Though As methylation is widespread in bacteria, fungi, algae, animals and humans, probably as a detoxification process, As methylation
Mammalian AS3MT is homologous to bacterial ArsM (
Expression of ArsM gene in rice may catalyze As methylation and volatilization, thus providing a strategy to reduce accumulation of toxic As species and/or total As in rice grains.
Although critical genes responsible for As uptake, transport and detoxification can reduce As accumulation in rice grains, limited natural genetic resources may ultimately restrict their application. In this context, gene-editing technologies are of great interest to both gene function characterization and crop improvement. The RNA-guided CRISPR/Cas9 system, which depends on bacterial Cluster Regularly Interspaced Short Palindromic Repeats (CRISPR)-associated nuclease (Cas), is emerging as the tool of choice for precise gene editing (
To produce low-As rice, critical genes that are responsible for As uptake and transport (e.g.,
Reducing the levels of the ubiquitous carcinogenic As in rice is a major public health goal. Arsenic levels and species vary widely in paddy soils for different regions and within different rice cultivars. During the past decade, molecular biology research on how plants deal with As has opened up unprecedented opportunities to make the rice grains safer by lowering its As content. Research using transgenic systems can inform plant breeders to select certain genetic markers over others to obtain low-As rice varieties. In addition, newly developed gene-editing technology can also help in altering endogenous genes (
YCh wrote the article, prepared the illustrations and incorporated edits from co-authors, and approved the final draft. Y-HH, YCa, and Y-GZ provided intellectual content and editorial suggestions for the manuscript. BR and LM conceptualized the overall structure of the review article, critically edited it and approved the final draft.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank Dr. Charlie Guy (University of Florida) for assistance with revising the manuscript. This work was supported by Jiangsu Provincial Natural Science Foundation of China (No. BK20160649), the Key Program of National Natural Science Foundation of China (Grant No. 21637002), China Postdoctoral Science Foundation (No. 2015M571735), Program B for Outstanding Ph.D. Candidates of Nanjing University (201601B010) and Jiangsu Planned Projects for Postdoctoral Research Funds (No. 1402004C).