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Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds

BACKGROUND: Peroxiredoxins (PRXs) have recently been identified as plant antioxidants. Completion of various genome sequencing projects has provided genome-wide information about PRX genes in major plant species. Two of these -- Oryza sativa (rice) and Arabidopsis -- each have 10 PRX members. Althou...

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Autores principales: Gho, Yun-Shil, Park, Sun-A, Kim, Sung-Ruyl, Chandran, Anil Kumar Nalini, An, Gynheung, Jung, Ki-Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5483221/
https://www.ncbi.nlm.nih.gov/pubmed/28647924
http://dx.doi.org/10.1186/s12284-017-0170-5
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author Gho, Yun-Shil
Park, Sun-A
Kim, Sung-Ruyl
Chandran, Anil Kumar Nalini
An, Gynheung
Jung, Ki-Hong
author_facet Gho, Yun-Shil
Park, Sun-A
Kim, Sung-Ruyl
Chandran, Anil Kumar Nalini
An, Gynheung
Jung, Ki-Hong
author_sort Gho, Yun-Shil
collection PubMed
description BACKGROUND: Peroxiredoxins (PRXs) have recently been identified as plant antioxidants. Completion of various genome sequencing projects has provided genome-wide information about PRX genes in major plant species. Two of these -- Oryza sativa (rice) and Arabidopsis -- each have 10 PRX members. Although significant progress has been made in understanding their biological roles in Arabidopsis, those functions in rice, a model crop plant, have not been well studied. RESULTS: We performed a comparative expression analysis of rice and Arabidopsis PRXs. Our phylogenetic analysis revealed that one subgroup contains three rice and three Arabidopsis Type-II PRXs that are expressed ubiquitously. This suggests that they are involved in housekeeping functions to process reactive oxygen species (ROS). Within the second subgroup, expression of Os1-CysPrxA (LOC_Os7g44430) and AtOs1-CysPrx is conserved in seeds while Os1-CysPrxB (LOC_Os7g44440) shows a root-preferential pattern of expression. We used transgenic plants expressing the GUS reporter gene under the control of the promoters of these two tandem duplicates to confirm their meta-expression patterns. Our GUS expression data from developing seeds and those that were germinating indicated that Os1-CysPrxB is involved in root development, as initiated from the embryo, while Os1-CysPrxA has roles in regulating endosperm development near the aleurone layer. For the third and fourth subgroups, the rice PRXs are more likely to show leaf/shoot-preferential expression, while those from Arabidopsis are significantly expressed in the flowers and seeds in addition to the leaf/shoot. To determine the biological meaning of those expression patterns that were dominantly identified in rice PRXs, we analyzed three rice genes showing leaf/shoot-preferential expression in a mutant of the light-responsive 1-deoxy-D-xylulose 5-phosphate reductoisomerase (dxr) gene and found that two of them were significantly down-regulated in the mutant. CONCLUSION: A global expression analysis of the PRX family in rice identified tandem duplicates, Os1-CysPrxA and Os1-CysPrxB, in the 1-CysPrx subgroup that are differentially expressed in developing seeds and germinating seeds. Analysis of the cis-acting regulatory elements (CREs) revealed unique CREs responsible for embryo and root or endosperm-preferential expression. In addition, the presence of leaf/shoot-preferential PRXs in rice suggests that they are required in that crop because those plants must tolerate a higher light intensity in their normal growth environment when compared with that of Arabidopsis. Downregulation of two PRXs in the dxr mutant causing an albino phenotype, implying that those genes have roles in processing ROS produced during photosynthesis. Network analysis of four PRXs allowed us to model regulatory pathways that explain the underlying protein interaction network. This will be a useful hypothetical model for further study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12284-017-0170-5) contains supplementary material, which is available to authorized users.
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spelling pubmed-54832212017-07-10 Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds Gho, Yun-Shil Park, Sun-A Kim, Sung-Ruyl Chandran, Anil Kumar Nalini An, Gynheung Jung, Ki-Hong Rice (N Y) Original Article BACKGROUND: Peroxiredoxins (PRXs) have recently been identified as plant antioxidants. Completion of various genome sequencing projects has provided genome-wide information about PRX genes in major plant species. Two of these -- Oryza sativa (rice) and Arabidopsis -- each have 10 PRX members. Although significant progress has been made in understanding their biological roles in Arabidopsis, those functions in rice, a model crop plant, have not been well studied. RESULTS: We performed a comparative expression analysis of rice and Arabidopsis PRXs. Our phylogenetic analysis revealed that one subgroup contains three rice and three Arabidopsis Type-II PRXs that are expressed ubiquitously. This suggests that they are involved in housekeeping functions to process reactive oxygen species (ROS). Within the second subgroup, expression of Os1-CysPrxA (LOC_Os7g44430) and AtOs1-CysPrx is conserved in seeds while Os1-CysPrxB (LOC_Os7g44440) shows a root-preferential pattern of expression. We used transgenic plants expressing the GUS reporter gene under the control of the promoters of these two tandem duplicates to confirm their meta-expression patterns. Our GUS expression data from developing seeds and those that were germinating indicated that Os1-CysPrxB is involved in root development, as initiated from the embryo, while Os1-CysPrxA has roles in regulating endosperm development near the aleurone layer. For the third and fourth subgroups, the rice PRXs are more likely to show leaf/shoot-preferential expression, while those from Arabidopsis are significantly expressed in the flowers and seeds in addition to the leaf/shoot. To determine the biological meaning of those expression patterns that were dominantly identified in rice PRXs, we analyzed three rice genes showing leaf/shoot-preferential expression in a mutant of the light-responsive 1-deoxy-D-xylulose 5-phosphate reductoisomerase (dxr) gene and found that two of them were significantly down-regulated in the mutant. CONCLUSION: A global expression analysis of the PRX family in rice identified tandem duplicates, Os1-CysPrxA and Os1-CysPrxB, in the 1-CysPrx subgroup that are differentially expressed in developing seeds and germinating seeds. Analysis of the cis-acting regulatory elements (CREs) revealed unique CREs responsible for embryo and root or endosperm-preferential expression. In addition, the presence of leaf/shoot-preferential PRXs in rice suggests that they are required in that crop because those plants must tolerate a higher light intensity in their normal growth environment when compared with that of Arabidopsis. Downregulation of two PRXs in the dxr mutant causing an albino phenotype, implying that those genes have roles in processing ROS produced during photosynthesis. Network analysis of four PRXs allowed us to model regulatory pathways that explain the underlying protein interaction network. This will be a useful hypothetical model for further study. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12284-017-0170-5) contains supplementary material, which is available to authorized users. Springer US 2017-06-24 /pmc/articles/PMC5483221/ /pubmed/28647924 http://dx.doi.org/10.1186/s12284-017-0170-5 Text en © The Author(s). 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
spellingShingle Original Article
Gho, Yun-Shil
Park, Sun-A
Kim, Sung-Ruyl
Chandran, Anil Kumar Nalini
An, Gynheung
Jung, Ki-Hong
Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title_full Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title_fullStr Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title_full_unstemmed Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title_short Comparative Expression Analysis of Rice and Arabidopsis Peroxiredoxin Genes Suggests Conserved or Diversified Roles Between the Two Species and Leads to the Identification of Tandemly Duplicated Rice Peroxiredoxin Genes Differentially Expressed in Seeds
title_sort comparative expression analysis of rice and arabidopsis peroxiredoxin genes suggests conserved or diversified roles between the two species and leads to the identification of tandemly duplicated rice peroxiredoxin genes differentially expressed in seeds
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5483221/
https://www.ncbi.nlm.nih.gov/pubmed/28647924
http://dx.doi.org/10.1186/s12284-017-0170-5
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