Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells

Heme is involved in various biological processes as a cofactor of hemoproteins located in various organelles. In plant cells, heme is synthesized by two isoforms of plastid-localized ferrochelatase, FC1 and FC2. In this study, by characterizing Arabidopsis T-DNA insertional mutants, we showed that t...

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Main Authors: Nino Asuela Espinas, Koichi Kobayashi, Yasushi Sato, Nobuyoshi Mochizuki, Kaori Takahashi, Ryouichi Tanaka, Tatsuru Masuda
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01326/full
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author Nino Asuela Espinas
Nino Asuela Espinas
Koichi Kobayashi
Yasushi Sato
Nobuyoshi Mochizuki
Kaori Takahashi
Ryouichi Tanaka
Tatsuru Masuda
author_facet Nino Asuela Espinas
Nino Asuela Espinas
Koichi Kobayashi
Yasushi Sato
Nobuyoshi Mochizuki
Kaori Takahashi
Ryouichi Tanaka
Tatsuru Masuda
author_sort Nino Asuela Espinas
collection DOAJ
description Heme is involved in various biological processes as a cofactor of hemoproteins located in various organelles. In plant cells, heme is synthesized by two isoforms of plastid-localized ferrochelatase, FC1 and FC2. In this study, by characterizing Arabidopsis T-DNA insertional mutants, we showed that the allocation of heme is differentially regulated by ferrochelatase isoforms in plant cells. Analyses of weak (fc1-1) and null (fc1-2) mutants suggest that FC1-producing heme is required for initial growth of seedling development. In contrast, weak (fc2-1) and null (fc2-2) mutants of FC2 showed pale green leaves and retarded growth, indicating that FC2-producing heme is necessary for chloroplast development. During the initial growth stage, FC2 deficiency caused reduction of plastid cytochromes. In addition, although FC2 deficiency marginally affected the assembly of photosynthetic reaction center complexes, it caused relatively larger but insufficient light-harvesting antenna to reaction centers, resulting in lower efficiency of photosynthesis. In the later vegetative growth, however, fc2-2 recovered photosynthetic growth, showing that FC1-producing heme may complement the FC2 deficiency. On the other hand, reduced level of cytochromes in microsomal fraction was discovered in fc1-1, suggesting that FC1-producing heme is mainly allocated to extraplastidic organelles. Furthermore, the expression of FC1 is induced by the treatment of an elicitor flg22 while that of FC2 was reduced, and fc1-1 abolished the flg22-dependent induction of FC1 expression and peroxidase activity. Consequently, our results clarified that FC2 produces heme for the photosynthetic machinery in the chloroplast, while FC1 is the housekeeping enzyme providing heme cofactor to the entire cell. In addition, FC1 can partly complement FC2 deficiency and is also involved in defense against stressful conditions.
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spelling doaj.art-147d65bad4dc4632b9a5c6732df52b9f2022-12-21T17:49:06ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-08-01710.3389/fpls.2016.01326212725Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis CellsNino Asuela Espinas0Nino Asuela Espinas1Koichi Kobayashi2Yasushi Sato3Nobuyoshi Mochizuki4Kaori Takahashi5Ryouichi Tanaka6Tatsuru Masuda7The University of TokyoOkinawa Institute of Science and Technology Graduate UniversityThe University of TokyoEhime UniversityKyoto UniversityHokkaido UniversityHokkaido UniversityThe University of TokyoHeme is involved in various biological processes as a cofactor of hemoproteins located in various organelles. In plant cells, heme is synthesized by two isoforms of plastid-localized ferrochelatase, FC1 and FC2. In this study, by characterizing Arabidopsis T-DNA insertional mutants, we showed that the allocation of heme is differentially regulated by ferrochelatase isoforms in plant cells. Analyses of weak (fc1-1) and null (fc1-2) mutants suggest that FC1-producing heme is required for initial growth of seedling development. In contrast, weak (fc2-1) and null (fc2-2) mutants of FC2 showed pale green leaves and retarded growth, indicating that FC2-producing heme is necessary for chloroplast development. During the initial growth stage, FC2 deficiency caused reduction of plastid cytochromes. In addition, although FC2 deficiency marginally affected the assembly of photosynthetic reaction center complexes, it caused relatively larger but insufficient light-harvesting antenna to reaction centers, resulting in lower efficiency of photosynthesis. In the later vegetative growth, however, fc2-2 recovered photosynthetic growth, showing that FC1-producing heme may complement the FC2 deficiency. On the other hand, reduced level of cytochromes in microsomal fraction was discovered in fc1-1, suggesting that FC1-producing heme is mainly allocated to extraplastidic organelles. Furthermore, the expression of FC1 is induced by the treatment of an elicitor flg22 while that of FC2 was reduced, and fc1-1 abolished the flg22-dependent induction of FC1 expression and peroxidase activity. Consequently, our results clarified that FC2 produces heme for the photosynthetic machinery in the chloroplast, while FC1 is the housekeeping enzyme providing heme cofactor to the entire cell. In addition, FC1 can partly complement FC2 deficiency and is also involved in defense against stressful conditions.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01326/fullCytochromesFerrochelatasePhotosynthesisbiotic stressplastidheme allocation
spellingShingle Nino Asuela Espinas
Nino Asuela Espinas
Koichi Kobayashi
Yasushi Sato
Nobuyoshi Mochizuki
Kaori Takahashi
Ryouichi Tanaka
Tatsuru Masuda
Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
Frontiers in Plant Science
Cytochromes
Ferrochelatase
Photosynthesis
biotic stress
plastid
heme allocation
title Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
title_full Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
title_fullStr Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
title_full_unstemmed Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
title_short Allocation of Heme is Differentially Regulated by Ferrochelatase Isoforms in Arabidopsis Cells
title_sort allocation of heme is differentially regulated by ferrochelatase isoforms in arabidopsis cells
topic Cytochromes
Ferrochelatase
Photosynthesis
biotic stress
plastid
heme allocation
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01326/full
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