Ferroportin 3 is a dual-targeted mitochondrial/chloroplast iron exporter necessary for iron homeostasis in Arabidopsis

ABSTRACT Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the necessity of strict iron regulation in these organelles, much remains unknown about mitochondrial and chloroplast iron transport in plants. Here...

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Main Authors Kim, Leah J, Tsuyuki, Kaitlyn M, Hu, Fengling, Park, Emily Y, Zhang, Jingwen, Jennifer Gallegos Iraheta, Ju-Chen, Chia, Huang, Rong, Tucker, Avery E, Clyne, Madeline, Castellano, Claire, Kim, Angie, Chung, Daniel D, Daveiga, Christopher T, Parsons, Elizabeth M, Vatamaniuk, Olena K, Jeong, Jeeyon
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Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 07.11.2020
Cold Spring Harbor Laboratory
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Abstract ABSTRACT Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the necessity of strict iron regulation in these organelles, much remains unknown about mitochondrial and chloroplast iron transport in plants. Here, we propose that Arabidopsis Ferroportin 3 (FPN3) is an iron exporter dual-targeted to mitochondria and chloroplasts. FPN3 is expressed in shoots regardless of iron conditions, but its transcripts accumulate under iron deficiency in roots. fpn3 mutants cannot grow as well as wild type under iron-deficient conditions and shoot iron levels are reduced in fpn3 mutants compared to wild type. ICP-MS measurements show that iron levels in the mitochondria and chloroplasts are increased relative to wild type, consistent with the proposed role of FPN3 as a mitochondrial/plastid iron exporter. In iron deficient fpn3 mutants, abnormal mitochondrial ultrastructure was observed, whereas chloroplast ultrastructure was not affected, implying that FPN3 plays a critical role in the mitochondria. Overall, our study suggests that FPN3 is essential for optimal iron homeostasis. Significance statement Iron homeostasis must be tightly controlled in the mitochondria and chloroplasts, but iron trafficking in these organelles is not fully understood. Our work suggests that FPN3 is an iron exporter required for maintaining proper iron levels in mitochondria and chloroplasts. Furthermore, FPN3 is necessary for the optimal growth and normal mitochondrial ultrastructure under iron deficiency. This study reveals the physiological role of FPN3 and advances our understanding of iron regulation in mitochondria and chloroplasts. Competing Interest Statement The authors have declared no competing interest. Footnotes * ↵* Author for contact: jjeong{at}amherst.edu
AbstractList Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the necessity of strict iron regulation in these organelles, much remains unknown about mitochondrial and chloroplast iron transport in plants. Here, we propose that Arabidopsis Ferroportin 3 (FPN3) is an iron exporter dual-targeted to mitochondria and chloroplasts. FPN3 is expressed in shoots regardless of iron conditions, but its transcripts accumulate under iron deficiency in roots. fpn3 mutants cannot grow as well as wild type under iron-deficient conditions and shoot iron levels are reduced in fpn3 mutants compared to wild type. ICP-MS measurements show that iron levels in the mitochondria and chloroplasts are increased relative to wild type, consistent with the proposed role of FPN3 as a mitochondrial/plastid iron exporter. In iron deficient fpn3 mutants, abnormal mitochondrial ultrastructure was observed, whereas chloroplast ultrastructure was not affected, implying that FPN3 plays a critical role in the mitochondria. Overall, our study suggests that FPN3 is essential for optimal iron homeostasis. Iron homeostasis must be tightly controlled in the mitochondria and chloroplasts, but iron trafficking in these organelles is not fully understood. Our work suggests that FPN3 is an iron exporter required for maintaining proper iron levels in mitochondria and chloroplasts. Furthermore, FPN3 is necessary for the optimal growth and normal mitochondrial ultrastructure under iron deficiency. This study reveals the physiological role of FPN3 and advances our understanding of iron regulation in mitochondria and chloroplasts.
ABSTRACT Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the necessity of strict iron regulation in these organelles, much remains unknown about mitochondrial and chloroplast iron transport in plants. Here, we propose that Arabidopsis Ferroportin 3 (FPN3) is an iron exporter dual-targeted to mitochondria and chloroplasts. FPN3 is expressed in shoots regardless of iron conditions, but its transcripts accumulate under iron deficiency in roots. fpn3 mutants cannot grow as well as wild type under iron-deficient conditions and shoot iron levels are reduced in fpn3 mutants compared to wild type. ICP-MS measurements show that iron levels in the mitochondria and chloroplasts are increased relative to wild type, consistent with the proposed role of FPN3 as a mitochondrial/plastid iron exporter. In iron deficient fpn3 mutants, abnormal mitochondrial ultrastructure was observed, whereas chloroplast ultrastructure was not affected, implying that FPN3 plays a critical role in the mitochondria. Overall, our study suggests that FPN3 is essential for optimal iron homeostasis. Significance statement Iron homeostasis must be tightly controlled in the mitochondria and chloroplasts, but iron trafficking in these organelles is not fully understood. Our work suggests that FPN3 is an iron exporter required for maintaining proper iron levels in mitochondria and chloroplasts. Furthermore, FPN3 is necessary for the optimal growth and normal mitochondrial ultrastructure under iron deficiency. This study reveals the physiological role of FPN3 and advances our understanding of iron regulation in mitochondria and chloroplasts. Competing Interest Statement The authors have declared no competing interest. Footnotes * ↵* Author for contact: jjeong{at}amherst.edu
Author Clyne, Madeline
Jennifer Gallegos Iraheta
Ju-Chen, Chia
Huang, Rong
Kim, Leah J
Tucker, Avery E
Chung, Daniel D
Hu, Fengling
Vatamaniuk, Olena K
Parsons, Elizabeth M
Park, Emily Y
Jeong, Jeeyon
Tsuyuki, Kaitlyn M
Kim, Angie
Zhang, Jingwen
Castellano, Claire
Daveiga, Christopher T
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Keywords Ferroportin
Mitochondria
Iron
Transport
Chloroplast
Language English
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Snippet ABSTRACT Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the...
Mitochondria and chloroplasts are organelles with high iron demand that are particularly susceptible to iron-induced oxidative stress. Despite the necessity of...
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SubjectTerms Arabidopsis
Chloroplasts
Gene expression
Homeostasis
Iron
Mitochondria
Mutants
Organelles
Oxidative stress
Plant Biology
Shoots
Ultrastructure
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Title Ferroportin 3 is a dual-targeted mitochondrial/chloroplast iron exporter necessary for iron homeostasis in Arabidopsis
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https://www.biorxiv.org/content/10.1101/2020.07.15.203646
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