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, Yingxi Chen Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo , Tokyo 153-8902 , Search for other works by this author on: Oxford Academic Kohji Nishimura Department of Life Sciences, Faculty of Life and Environmental Sciences, Shimane University , Shimane 690-8504 , Japan Search for other works by this author on: Oxford Academic Mutsutomo Tokizawa Present address: Sustainable System Research Laboratory, Central Research Institute of Electric Power Industry, Chiba 270-1194, Japan. Search for other works by this author on: Oxford Academic Yoshiharu Y Yamamoto United Graduate School of Agricultural Science, Gifu University , Gifu 501-1193 , Japan Search for other works by this author on: Oxford Academic Yosh*to Oka Division of Biological Sciences, Graduate School of Science, Kyoto University , Kyoto 606-8501 , Japan Search for other works by this author on: Oxford Academic Tomonao Matsush*ta Division of Biological Sciences, Graduate School of Science, Kyoto University , Kyoto 606-8501 , Japan Search for other works by this author on: Oxford Academic Kousuke Hanada Department of Bioscience and Bioinformatics, Kyushu Institute of Technology , f*ckuoka 820-8502 , Japan Search for other works by this author on: Oxford Academic Kazumasa Shirai Department of Bioscience and Bioinformatics, Kyushu Institute of Technology , f*ckuoka 820-8502 , Japan Search for other works by this author on: Oxford Academic Shoji Mano Department of Evolutionary Biology and Biodiversity, National Institute for Basic Biology , Okazaki 444-8585 , Japan Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies) , Okazaki 444-8585 , Japan Search for other works by this author on: Oxford Academic Takayuki Shimizu Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo , Tokyo 153-8902 , Japan Present address: Faculty Division of Natural Sciences, Nara Women's University, Nara 630-8263, Japan. Search for other works by this author on: Oxford Academic
https://orcid.org/0000-0001-5798-749X Tatsuru Masuda Department of General Systems Studies, Graduate School of Arts and Sciences, The University of Tokyo , Tokyo 153-8902 , Japan Author for correspondence: cmasuda2@g.ecc.u-tokyo.ac.jp Search for other works by this author on: Oxford Academic
Published:
28 May 2024
Article history
Received:
09 February 2024
Accepted:
25 April 2024
Published:
28 May 2024
Corrected and typeset:
30 May 2024
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Yingxi Chen, Kohji Nishimura, Mutsutomo Tokizawa, Yoshiharu Y Yamamoto, Yosh*to Oka, Tomonao Matsush*ta, Kousuke Hanada, Kazumasa Shirai, Shoji Mano, Takayuki Shimizu, Tatsuru Masuda, Alternative localization of HEME OXYGENASE 1 in plant cells regulates cytosolic heme catabolism, Plant Physiology, 2024;, kiae288, https://doi.org/10.1093/plphys/kiae288
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Abstract
Heme, an organometallic tetrapyrrole, is widely engaged in oxygen transport, electron delivery, enzymatic reactions, and signal transduction. In plants, it is also involved in photomorphogenesis and photosynthesis. HEME OXYGENASE 1 (HO1) initiates the first committed step in heme catabolism, and it has generally been thought that this reaction takes place in chloroplasts. Here, we show that HO1 in both Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa) has 2 transcription start sites (TSSs), producing long (HO1L) and short (HO1S) transcripts. Their products localize to the chloroplast and the cytosol, respectively. During early development or de-etiolation, the HO1L/HO1S ratio gradually increases. Light perception via phytochromes (Phys) and cryptochromes elevates the HO1L/HO1S ratio in the whole seedling through the functions of ELONGATED HYPOCOTYL 5 (HY5) and HY5 hom*oLOG and through the suppression of DE-ETIOLATED 1, CONSTITUTIVE PHOTOMORPHOGENESIS 1, and PHYTOCHROME INTERACTING FACTORs. HO1L introduction complements the HO1-deficient mutant; surprisingly, HO1S expression also restores the short hypocotyl phenotype and high pigment content and helps the mutant recover from the genomes uncoupled (gun) phenotype. This indicates the assembly of functional Phys within these lines. Furthermore, our findings support the hypothesis that a mobile heme signal is involved in retrograde signaling from the chloroplast. Altogether, our work clarifies the molecular mechanism of HO1 TSS regulation and highlights the presence of a cytosolic bypass for heme catabolism in plant cells.
© The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.
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