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Journal ArticleDOI

Preferential Delivery of Zinc to Developing Tissues in Rice Is Mediated by P-Type Heavy Metal ATPase OsHMA2

01 Jun 2013-Plant Physiology (American Society of Plant Biologists)-Vol. 162, Iss: 2, pp 927-939
TL;DR: Rice (Oryza sativa) heavy metal ATPase2 (OsHMA2), a member of P-type ATPases, is involved in preferential delivery of zinc to the developing tissues in rice and plays an important role in preferential distribution of zinc as well as cadmium through the phloem to the developed tissues.
Abstract: Developing tissues such as meristems and reproductive organs require high zinc, but the molecular mechanisms of how zinc taken up by the roots is preferentially delivered to these tissues with low transpiration are unknown. Here, we report that rice (Oryza sativa) heavy metal ATPase2 (OsHMA2), a member of P-type ATPases, is involved in preferential delivery of zinc to the developing tissues in rice. OsHMA2 was mainly expressed in the mature zone of the roots at the vegetative stage, but higher expression was also found in the nodes at the reproductive stage. The expression was unaffected by either zinc deficiency or zinc excess. OsHMA2 was localized at the pericycle of the roots and at the phloem of enlarged and diffuse vascular bundles in the nodes. Heterologous expression of OsHMA2 in yeast (Saccharomyces cerevisiae) showed influx transport activity for zinc as well as cadmium. Two independent Tos17 insertion lines showed decreased zinc concentration in the crown root tips, decreased concentration of zinc and cadmium in the upper nodes and reproductive organs compared with wild-type rice. Furthermore, a short-term labeling experiment with 67Zn showed that the distribution of zinc to the panicle and uppermost node I was decreased, but that, to the lower nodes, was increased in the two mutants. Taken together, OsHMA2 in the nodes plays an important role in preferential distribution of zinc as well as cadmium through the phloem to the developing tissues.

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Citations
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Journal ArticleDOI
TL;DR: Proteins mediating the uptake of arsenic and cadmium have been identified, and the speciation and biotransformations of arsenic are now understood, and factors controlling the efficiency of root-to-shoot translocation and the partitioning of toxic elements through the rice node have also been identified.
Abstract: Arsenic, cadmium, lead, and mercury are toxic elements that are almost ubiquitously present at low levels in the environment because of anthropogenic influences. Dietary intake of plant-derived food represents a major fraction of potentially health-threatening human exposure, especially to arsenic and cadmium. In the interest of better food safety, it is important to reduce toxic element accumulation in crops. A molecular understanding of the pathways responsible for this accumulation can enable the development of crop varieties with strongly reduced concentrations of toxic elements in their edible parts. Such understanding is rapidly progressing for arsenic and cadmium but is in its infancy for lead and mercury. Basic discoveries have been made in Arabidopsis, rice, and other models, and most advances in crops have been made in rice. Proteins mediating the uptake of arsenic and cadmium have been identified, and the speciation and biotransformations of arsenic are now understood. Factors controlling the efficiency of root-to-shoot translocation and the partitioning of toxic elements through the rice node have also been identified.

745 citations


Cites background from "Preferential Delivery of Zinc to De..."

  • ...In contrast to other HMA members, HMA2 has been hypothesized to function as an influx transporter (140) (Figure 1)....

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  • ...A reduction in OsHMA2 activity resulting from transposon insertion or RNA interference (RNAi) decreases the translocation of Cd to the shoot (112, 119, 140)....

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  • ...Loss of function resulted not only in a reduction of grain Cd but also in a reduction of grain Zn (140)....

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  • ...OsHMA2 is expressed not only in roots but also in the upper nodes during the reproductive stage (140)....

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Journal ArticleDOI
TL;DR: A member of the Oryza sativa C-type ATP-binding cassette transporter (OsABCC) family, OsABCC1, is involved in the detoxification and reduction of As in rice grains and was expressed in many organs, including the roots, leaves, nodes, peduncle, and rachis.
Abstract: Arsenic (As) is a chronic poison that causes severe skin lesions and cancer. Rice (Oryza sativa L.) is a major dietary source of As; therefore, reducing As accumulation in the rice grain and thereby diminishing the amount of As that enters the food chain is of critical importance. Here, we report that a member of the Oryza sativa C-type ATP-binding cassette (ABC) transporter (OsABCC) family, OsABCC1, is involved in the detoxification and reduction of As in rice grains. We found that OsABCC1 was expressed in many organs, including the roots, leaves, nodes, peduncle, and rachis. Expression was not affected when plants were exposed to low levels of As but was up-regulated in response to high levels of As. In both the basal nodes and upper nodes, which are connected to the panicle, OsABCC1 was localized to the phloem region of vascular bundles. Furthermore, OsABCC1 was localized to the tonoplast and conferred phytochelatin-dependent As resistance in yeast. Knockout of OsABCC1 in rice resulted in decreased tolerance to As, but did not affect cadmium toxicity. At the reproductive growth stage, the As content was higher in the nodes and in other tissues of wild-type rice than in those of OsABCC1 knockout mutants, but was significantly lower in the grain. Taken together, our results indicate that OsABCC1 limits As transport to the grains by sequestering As in the vacuoles of the phloem companion cells of the nodes in rice.

357 citations


Cites background or result from "Preferential Delivery of Zinc to De..."

  • ...S4), matched the results from the previous reports (25, 26) and indicated the purity of the tissues sampled....

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  • ...In contrast to Cd, which is likely sequestered by OsHMA3 into the vacuoles in the ionic form and loaded into the xylem in the same form by other transporter(s) (26, 29), As is sequestered by OsABCC1 into the root vacuoles most likely in the form of As–PC complexes (Fig....

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Journal ArticleDOI
TL;DR: A number of countermeasures to address soil Cd contamination are proposed, including i) mitigation of Cd transfer from paddy soils to rice grain, and ii) intervention in those farmers who consume home-grown Cd-contaminated rice.

324 citations

Journal ArticleDOI
TL;DR: The beneficial effects of Se on plants under Cd stress, and how it can minimize or mitigate Cd toxicity in plants is discussed.
Abstract: Cd is the third major contaminant of greatest hazard to the environment after mercury and lead and is considered as the only metal that poses health risks to both humans and animals at plant tissue concentrations that are generally not phytotoxic. Cd accumulation in plant shoots depends on Cd entry through the roots, sequestration within root vacuoles, translocation in the xylem and phloem, and Cd dilution within the plant shoot throughout its growth. Several metal transporters, processes, and channels are involved from the first step of Cd reaching the root cells and until its final accumulation in the edible parts of the plant. It is hard to demonstrate one step as the pivotal factor to decide the Cd tolerance or accumulation ability of plants since the role of a specific transporter/process varies among plant species and even cultivars. In this review, we discuss the sources of Cd pollutants, Cd toxicity to plants, and mechanisms of Cd uptake and redistribution in plant tissues. The metal transporters involved in Cd transport within plant tissues are also discussed and how their manipulation can control Cd uptake and/or translocation. Finally, we discuss the beneficial effects of Se on plants under Cd stress, and how it can minimize or mitigate Cd toxicity in plants.

319 citations

Journal ArticleDOI
TL;DR: In this paper, the authors reviewed recent progress in understanding the biogeochemical processes controlling As and Cd bioavailability in paddy soil, the mechanisms of their uptake, translocation and detoxification in rice plants, and strategies to reduce their accumulation in rice grain.
Abstract: Arsenic (As) and cadmium (Cd) are two toxic elements that have a relatively high risk of transfer from paddy soil to rice grain. Rice is a major dietary source of these two elements for populations consuming rice as a staple food. Reducing their accumulation in rice grain is important for food safety and human health. We review recent progress in understanding the biogeochemical processes controlling As and Cd bioavailability in paddy soil, the mechanisms of their uptake, translocation and detoxification in rice plants, and strategies to reduce their accumulation in rice grain. Similarities and differences between the two elements are emphasized. Some knowledge gaps are also identified. The concentrations of As and Cd in rice grain vary by three orders of magnitude, depending on the bioavailability of the two elements in soil, rice genotype and growing conditions. The redox potential in paddy soil has a profound but opposite effect on As and Cd bioavailability, whereas soil pH affects Cd bioavailability more than As bioavailability. A number of key genes involved in As and Cd uptake, translocation, sequestration, and detoxification in rice have been characterized. Allelic variations of several genes underlying the variations in Cd accumulation have been identified, but more remains to be elucidated, especially for As. Two types of strategies can be used to reduce As and Cd accumulation, reducing their bioavailability in soil or their uptake and translocation in rice. Reducing the accumulation of both As and Cd in rice simultaneously remains a great challenge.

272 citations

References
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Journal ArticleDOI
TL;DR: A large number of morphologically normal, fertile, transgenic rice plants were obtained by co-cultivation of rice tissues with Agrobacterium tumefaciens, and sequence analysis revealed that the boundaries of the T-DNA in transgenic Rice plants were essentially identical to those intransgenic dicotyledons.
Abstract: Summary A large number of morphologically normal, fertile, transgenic rice plants were obtained by co-cultivation of rice tissues with Agrobacterium tumefaciens The efficiency of transformation was similar to that obtained by the methods used routinely for transformation of dicotyledons with the bacterium Stable integration, expression and inheritance of transgenes were demonstrated by molecular and genetic analysis of transformants in the R0, R1 and R2 generations Sequence analysis revealed that the boundaries of the T-DNA in transgenic rice plants were essentially identical to those in transgenic dicotyledons Calli induced from scutella were very good starting materials A strain of A tumefaciens that carried a so-called ‘super-binary’ vector gave especially high frequencies of transformation of various cultivars of japonica rice that included Koshihikari, which normally shows poor responses in tissue culture

3,475 citations


"Preferential Delivery of Zinc to De..." refers methods in this paper

  • ...Transgenic Rice Carrying OsHMA2 Promoter-GFP To investigate the cellular expression of OsHMA2, we introduced a construct consisting of the promoter (2.13 kb) of OsHMA2 fused with GFP to rice using an Agrobacterium tumefaciens-mediated transformation system (Hiei et al., 1994)....

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Book
15 Jun 2021
TL;DR: The third edition of Marschner's "Mineral Nutrition of Higher Plants" as mentioned in this paper is the most comprehensive and comprehensive reference on plant mineral nutrition, which has been published since 1996.
Abstract: Respected and known worldwide in the field for his research in plant nutrition, Dr. Horst Marschner authored two editions of Mineral Nutrition of Higher Plants. His research greatly advanced the understanding of rhizosphere processes and trace element uptake by plants and he published extensively in a variety of plant nutrition areas. While doing agricultural research in West Africa in 1996, Dr. Marschner contracted malaria and passed away, and until now this legacy title went unrevised. Despite the passage of time, it remains the definitive reference on plant mineral nutrition. Great progress has been made in the understanding of various aspects of plant nutrition and in recent years the view on the mode of action of mineral nutrients in plant metabolism and yield formation has shifted. Nutrients are not only viewed as constituents of plant compounds (constructing material), enzymes and electron transport chains but also as signals regulating plant metabolism via complex signal transduction networks. In these networks, phytohormones also play an important role. Principles of the mode of action of phytohormones and examples of the interaction of hormones and mineral nutrients on source and sink strength and yield formation are discussed in this edition. Phytohormones have a role as chemical messengers (internal signals) to coordinate development and responses to environmental stimuli at the whole plant level. These and many other molecular developments are covered in the long-awaited new edition. Esteemed plant nutrition expert and Horst Marschner's daughter, Dr. Petra Marschner, together with a team of key co-authors who worked with Horst Marschner on his research, now present a thoroughly updated and revised third edition of Marschner's Mineral Nutrition of Higher Plants, maintaining its value for plant nutritionists worldwide. Key Features * Second Edition of this established text * Structure of the book remains the same * 50% of the reference and 50% of the figures and tables have been replaced * Whole of the text has been revised * Coverage of plant (soil interactions has been increased considerably)

3,040 citations


"Preferential Delivery of Zinc to De..." refers background in this paper

  • ...Therefore, zinc deficiency in plants causes stunted growth and “little leaf” (Broadley et al., 2011)....

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  • ...In plants, zinc is involved in many enzyme activities, maintenance of integrity of biomembranes, RNA and DNA metabolism, carbohydrate metabolism, cell division, protein synthesis, gene expression regulation, and so on (Broadley et al., 2011)....

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Journal ArticleDOI
TL;DR: Information on where in the plant each of the ZIP transporters functions and how each is controlled in response to nutrient availability may allow the manipulation of plant mineral status with an eye to creating food crops with enhanced mineral content, and developing crops that bioaccumulate or exclude toxic metals.

1,068 citations


"Preferential Delivery of Zinc to De..." refers background in this paper

  • ...Zinc is taken up by the roots through the ZIP (for ZRT, IRT-related proteins) transporters (Grotz et al., 1998; Guerinot, 2000)....

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Journal ArticleDOI
TL;DR: In this article, a member of the Nramp (for the Natural Resistance-associated Macrophage Protein) family (Nramp5) was found to be involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice.
Abstract: Paddy rice (Oryza sativa) is able to accumulate high concentrations of Mn without showing toxicity; however, the molecular mechanisms underlying Mn uptake are unknown. Here, we report that a member of the Nramp (for the Natural Resistance-Associated Macrophage Protein) family, Nramp5, is involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice. Nramp5 was constitutively expressed in the roots and encodes a plasma membrane–localized protein. Nramp5 was polarly localized at the distal side of both exodermis and endodermis cells. Knockout of Nramp5 resulted in a significant reduction in growth and grain yield, especially when grown at low Mn concentrations. This growth reduction could be partially rescued by supplying high concentrations of Mn but not by the addition of Fe. Mineral analysis showed that the concentration of Mn and Cd in both the roots and shoots was lower in the knockout line than in wild-type rice. A short-term uptake experiment revealed that the knockout line lost the ability to take up Mn and Cd. Taken together, Nramp5 is a major transporter of Mn and Cd and is responsible for the transport of Mn and Cd from the external solution to root cells.

829 citations


"Preferential Delivery of Zinc to De..." refers background in this paper

  • ...Recently, a member of the Nramp family, Nramp5, was identified as a major transporter for cadmium uptake in rice (Sasaki et al., 2012)....

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Journal ArticleDOI
TL;DR: The cloning of the first zinc transporter genes from plants, the ZIP1, ZIP2, and ZIP3 genes of Arabidopsis thaliana, define a family of metal ion transporters that are found in plants, protozoa, fungi, invertebrates, and vertebrates, making it now possible to address questions ofMetal ion accumulation and homeostasis in diverse organisms.
Abstract: Millions of people worldwide suffer from nutritional imbalances of essential metals like zinc. These same metals, along with pollutants like cadmium and lead, contaminate soils at many sites around the world. In addition to posing a threat to human health, these metals can poison plants, livestock, and wildlife. Deciphering how metals are absorbed, transported, and incorporated as protein cofactors may help solve both of these problems. For example, edible plants could be engineered to serve as better dietary sources of metal nutrients, and other plant species could be tailored to remove metal ions from contaminated soils. We report here the cloning of the first zinc transporter genes from plants, the ZIP1, ZIP2, and ZIP3 genes of Arabidopsis thaliana. Expression in yeast of these closely related genes confers zinc uptake activities. In the plant, ZIP1 and ZIP3 are expressed in roots in response to zinc deficiency, suggesting that they transport zinc from the soil into the plant. Although expression of ZIP2 has not been detected, a fourth related Arabidopsis gene identified by genome sequencing, ZIP4, is induced in both shoots and roots of zinc-limited plants. Thus, ZIP4 may transport zinc intracellularly or between plant tissues. These ZIP proteins define a family of metal ion transporters that are found in plants, protozoa, fungi, invertebrates, and vertebrates, making it now possible to address questions of metal ion accumulation and homeostasis in diverse organisms.

698 citations


"Preferential Delivery of Zinc to De..." refers background in this paper

  • ...Zinc is taken up by the roots through the ZIP (for ZRT, IRT-related proteins) transporters (Grotz et al., 1998; Guerinot, 2000)....

    [...]