OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice

Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance‐associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP...

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Published inPlant, cell and environment Vol. 43; no. 10; pp. 2476 - 2491
Main Authors Chang, Jia‐Dong, Huang, Sheng, Yamaji, Naoki, Zhang, Wenwen, Ma, Jian Feng, Zhao, Fang‐Jie
Format Journal Article
LanguageEnglish
Published Chichester, UK John Wiley & Sons, Ltd 01.10.2020
Wiley Subscription Services, Inc
Subjects
Online AccessGet full text
ISSN0140-7791
1365-3040
1365-3040
DOI10.1111/pce.13843

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Abstract Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance‐associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane‐localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant. Rice is the major dietary source of the toxic metal cadmium. Understand how rice takes up Cd is important. Two previous studies showed that OsNRAMP1 could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays, but its in planta function remains unknown. Here, we functionally characterize OsNRAMP1 and show that the transporter contributes significantly to the uptake of Cd and Mn in rice, but not the uptake of Fe or As. OsNRAMP1 and OsNRAMP5 play similar but non‐redundant functions. Our study sheds light on the mechanisms of Cd and Mn uptake by rice.
AbstractList Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane-localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant.
Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance‐associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane‐localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5 , while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant. Rice is the major dietary source of the toxic metal cadmium. Understand how rice takes up Cd is important. Two previous studies showed that OsNRAMP1 could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays, but its in planta function remains unknown. Here, we functionally characterize OsNRAMP1 and show that the transporter contributes significantly to the uptake of Cd and Mn in rice, but not the uptake of Fe or As. OsNRAMP1 and OsNRAMP5 play similar but non‐redundant functions. Our study sheds light on the mechanisms of Cd and Mn uptake by rice.
Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane-localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant.Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane-localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant.
Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance‐associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane‐localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant. Rice is the major dietary source of the toxic metal cadmium. Understand how rice takes up Cd is important. Two previous studies showed that OsNRAMP1 could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays, but its in planta function remains unknown. Here, we functionally characterize OsNRAMP1 and show that the transporter contributes significantly to the uptake of Cd and Mn in rice, but not the uptake of Fe or As. OsNRAMP1 and OsNRAMP5 play similar but non‐redundant functions. Our study sheds light on the mechanisms of Cd and Mn uptake by rice.
Author Huang, Sheng
Ma, Jian Feng
Yamaji, Naoki
Chang, Jia‐Dong
Zhang, Wenwen
Zhao, Fang‐Jie
Author_xml – sequence: 1
  givenname: Jia‐Dong
  orcidid: 0000-0002-4415-033X
  surname: Chang
  fullname: Chang, Jia‐Dong
  organization: Nanjing Agricultural University
– sequence: 2
  givenname: Sheng
  surname: Huang
  fullname: Huang, Sheng
  organization: Okayama University
– sequence: 3
  givenname: Naoki
  surname: Yamaji
  fullname: Yamaji, Naoki
  organization: Okayama University
– sequence: 4
  givenname: Wenwen
  surname: Zhang
  fullname: Zhang, Wenwen
  organization: Nanjing Agricultural University
– sequence: 5
  givenname: Jian Feng
  orcidid: 0000-0003-3411-827X
  surname: Ma
  fullname: Ma, Jian Feng
  organization: Okayama University
– sequence: 6
  givenname: Fang‐Jie
  orcidid: 0000-0002-0164-169X
  surname: Zhao
  fullname: Zhao, Fang‐Jie
  email: fangjie.zhao@njau.edu.cn
  organization: Nanjing Agricultural University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32666540$$D View this record in MEDLINE/PubMed
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Issue 10
Keywords OsNRAMP1
food safety
cadmium
rice
manganese
metal transporter
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Snippet Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance‐associated...
Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated...
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SubjectTerms Arsenic
Cadmium
Cadmium - metabolism
Cation Transport Proteins - metabolism
environment
food safety
Gene Knockdown Techniques
Heavy metals
Iron
Iron deficiency
Leaves
Macrophages
Manganese
Manganese - metabolism
Membrane proteins
Mesophyll
metal transporter
Microorganisms, Genetically-Modified
nutrient deficiencies
Oryza - metabolism
OsNRAMP1
Plant Proteins - metabolism
Plants, Genetically Modified
Protein transport
Proteins
Rice
Saccharomyces cerevisiae
Shoots
toxicity
Transcriptome
Yeast
yeasts
Title OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpce.13843
https://www.ncbi.nlm.nih.gov/pubmed/32666540
https://www.proquest.com/docview/2444218249
https://www.proquest.com/docview/2424097831
https://www.proquest.com/docview/2524266005
Volume 43
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