chlB Requirement for Chlorophyll Biosynthesis under Short Photoperiod in Marchantia polymorpha L.
Abstract
Chlorophylls (Chls) play pivotal roles in energy absorption and transduction and also in charge separation in reaction centers in all photosynthetic organisms. In Chl biosynthesis steps, only a step for the enzymatic reduction of protochlorophyllide (Pchlide) to chlorophyllide (Chlide) is mediated by both nuclear- and chloroplast-encoded genes in land plants. Many plants encode the genes for light-dependent Pchlide reductase (LPOR) and light-independent Pchlide reductase (DPOR) in the nucleus and chloroplast genome, respectively. During the diversification of land plants, the reduction step of Pchlide to Chlide has become solely dependent on LPOR, and the genes for DPOR have been lost from chloroplast genome. It remains unclear why DPOR persists in some land plants, how they were eliminated from chloroplast genomes during the diversification of land plants, and under what environmental conditions DPOR was required. We demonstrate that DPOR is functional in liverwort (Marchantia polymorpha L.) and plays an important role in Chl biosynthesis. Having established a plastid transformation system in liverwort, we disrupted chlB, which encodes a subunit of DPOR in the M. polymorpha chloroplast genome. Morphological and Chl content analysis of a chlB mutant grown under different photoperiods revealed that DPOR is particularly required for Chl biosynthesis under short-day conditions.more »
- Authors:
-
- Kyoto Univ. (Japan). Graduate School of Science. Dept. of Botany
- Hokkaido Univ., Sapporo (Japan). Inst. of Low Temperature Science
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Japan Society for the Promotion of Science (JSPS)
- OSTI Identifier:
- 1625333
- Grant/Contract Number:
- AC02-05CH11231; 25650126
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology and Evolution
- Additional Journal Information:
- Journal Volume: 6; Journal Issue: 3; Journal ID: ISSN 1759-6653
- Publisher:
- Society for Molecular Biology and Evolution
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; Evolutionary Biology; Genetics & Heredity; plastid transformation; chloroplast genome evolution; bryophyte; chlorophyll metabolism
Citation Formats
Ueda, Minoru, Tanaka, Ayumi, Sugimoto, Kazuhiko, Shikanai, Toshiharu, and Nishimura, Yoshiki. chlB Requirement for Chlorophyll Biosynthesis under Short Photoperiod in Marchantia polymorpha L.. United States: N. p., 2014.
Web. doi:10.1093/gbe/evu045.
Ueda, Minoru, Tanaka, Ayumi, Sugimoto, Kazuhiko, Shikanai, Toshiharu, & Nishimura, Yoshiki. chlB Requirement for Chlorophyll Biosynthesis under Short Photoperiod in Marchantia polymorpha L.. United States. https://doi.org/10.1093/gbe/evu045
Ueda, Minoru, Tanaka, Ayumi, Sugimoto, Kazuhiko, Shikanai, Toshiharu, and Nishimura, Yoshiki. Thu .
"chlB Requirement for Chlorophyll Biosynthesis under Short Photoperiod in Marchantia polymorpha L.". United States. https://doi.org/10.1093/gbe/evu045. https://www.osti.gov/servlets/purl/1625333.
@article{osti_1625333,
title = {chlB Requirement for Chlorophyll Biosynthesis under Short Photoperiod in Marchantia polymorpha L.},
author = {Ueda, Minoru and Tanaka, Ayumi and Sugimoto, Kazuhiko and Shikanai, Toshiharu and Nishimura, Yoshiki},
abstractNote = {Chlorophylls (Chls) play pivotal roles in energy absorption and transduction and also in charge separation in reaction centers in all photosynthetic organisms. In Chl biosynthesis steps, only a step for the enzymatic reduction of protochlorophyllide (Pchlide) to chlorophyllide (Chlide) is mediated by both nuclear- and chloroplast-encoded genes in land plants. Many plants encode the genes for light-dependent Pchlide reductase (LPOR) and light-independent Pchlide reductase (DPOR) in the nucleus and chloroplast genome, respectively. During the diversification of land plants, the reduction step of Pchlide to Chlide has become solely dependent on LPOR, and the genes for DPOR have been lost from chloroplast genome. It remains unclear why DPOR persists in some land plants, how they were eliminated from chloroplast genomes during the diversification of land plants, and under what environmental conditions DPOR was required. We demonstrate that DPOR is functional in liverwort (Marchantia polymorpha L.) and plays an important role in Chl biosynthesis. Having established a plastid transformation system in liverwort, we disrupted chlB, which encodes a subunit of DPOR in the M. polymorpha chloroplast genome. Morphological and Chl content analysis of a chlB mutant grown under different photoperiods revealed that DPOR is particularly required for Chl biosynthesis under short-day conditions. Our findings suggest that an environmental condition in the form of photoperiod is an important factor that determines the loss or retention of chloroplast-encoded genes mediating Pchlide reduction to Chlide.},
doi = {10.1093/gbe/evu045},
journal = {Genome Biology and Evolution},
number = 3,
volume = 6,
place = {United States},
year = {Thu Feb 27 00:00:00 EST 2014},
month = {Thu Feb 27 00:00:00 EST 2014}
}
Works referenced in this record:
Direct transformation of the liverwort Marchantia polymorpha L. by particle bombardment using immature thalli developing from spores
journal, June 2008
- Chiyoda, Shota; Ishizaki, Kimitsune; Kataoka, Hideo
- Plant Cell Reports, Vol. 27, Issue 9
Cloning, Nucleotide Sequences and Differential Expression of the nifH and nifH-Like (frxC) Genes from the Filamentous Nitrogen-Fixing Cyanobacterium Plectonema boryanum
journal, October 1991
- Fujita, Yuichi; Takahashi, Yasuhiro; Shonai, Fumio
- Plant and Cell Physiology, Vol. 32, Issue 7
Simple and efficient plastid transformation system for the liverwort Marchantia polymorpha L. suspension-culture cells
journal, November 2006
- Chiyoda, Shota; Linley, Philip J.; Yamato, Katsuyuki T.
- Transgenic Research, Vol. 16, Issue 1
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns
journal, November 2007
- Jansen, R. K.; Cai, Z.; Raubeson, L. A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
Bryophyte and Lichen Diversity Under Simulated Environmental Change Compared with Observed Variation in Unmanipulated Alpine Tundra
journal, March 2006
- Jägerbrand, Annika K.; Lindblad, Karin E. M.; Björk, Robert G.
- Biodiversity and Conservation, Vol. 15, Issue 14
Rapid Induction of Distinct Stress Responses after the Release of Singlet Oxygen in Arabidopsis
journal, October 2003
- op den Camp, R. G. L.
- THE PLANT CELL ONLINE, Vol. 15, Issue 10
Subfunctionalization of Sigma Factors during the Evolution of Land Plants Based on Mutant Analysis of Liverwort (Marchantia polymorpha L.) MpSIG1
journal, September 2013
- Ueda, Minoru; Takami, Tsuneaki; Peng, Lianwei
- Genome Biology and Evolution, Vol. 5, Issue 10
Identification of the chlB Gene and the Gene Product Essential for the Light-Independent Chlorophyll Biosynthesis in the Cyanobacterium Plectonema boryanum
journal, April 1996
- Fujita, Y.; Takagi, H.; Hase, T.
- Plant and Cell Physiology, Vol. 37, Issue 3
FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg ++ -branch of this pathway
journal, December 2011
- Kauss, Dominika; Bischof, Sylvain; Steiner, Sandro
- FEBS Letters, Vol. 586, Issue 3
Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC).
journal, August 1992
- Suzuki, J. Y.; Bauer, C. E.
- The Plant Cell, Vol. 4, Issue 8
Direct transformation and plant regeneration of the haploid liverwort Marchantia polymorpha L.
journal, June 2000
- Takenaka, Mizuki; Yamaoka, Shohei; Hanajiri, Tsutomu
- Transgenic Research, Vol. 9, Issue 3, p. 179-185
The Endosymbiont Hypothesis Revisited
book, January 1992
- Gray, Michael W.
- International Review of Cytology
Identification of a Vinyl Reductase Gene for Chlorophyll Synthesis in Arabidopsis thaliana and Implications for the Evolution of Prochlorococcus Species
journal, January 2005
- Nagata, Nozomi; Tanaka, Ryouichi; Satoh, Soichirou
- The Plant Cell, Vol. 17, Issue 1
No single way to understand singlet oxygen signalling in plants
journal, May 2008
- Kim, Chanhong; Meskauskiene, Rasa; Apel, Klaus
- EMBO reports, Vol. 9, Issue 5
Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA
journal, August 1986
- Ohyama, Kanji; Fukuzawa, Hideya; Kohchi, Takayuki
- Nature, Vol. 322, Issue 6079
Characterization of cDNA of the Liverwort Phytochrome Gene, and Phytochrome Involvement in the Light-Dependent and Light-Independent Protochlorophyllide Oxidoreductase Gene Expression in Marchantia paleacea var. diptera
journal, June 2001
- Suzuki, Takanori; Takio, Susumu; Yamamoto, Isamu
- Plant and Cell Physiology, Vol. 42, Issue 6
Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I
journal, August 1998
- Shikanai, Toshiharu; Endo, Tsuyoshi; Hashimoto, Takashi
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 16
Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms
journal, May 1998
- Armstrong, Gregory A.
- Journal of Photochemistry and Photobiology B: Biology, Vol. 43, Issue 2
The Major Route for Chlorophyll Synthesis Includes [3,8-divinyl]-chlorophyllide a Reduction in Arabidopsis thaliana
journal, October 2007
- Nagata, N.; Tanaka, R.; Tanaka, A.
- Plant and Cell Physiology, Vol. 48, Issue 12
Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus
journal, September 2002
- Martin, W.; Rujan, T.; Richly, E.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 19
Overexpression of light‐dependent PORA or PORB in plants depleted of endogenous POR by far‐red light enhances seedling survival in white light and protects against photooxidative damage
journal, September 1997
- Sperling, Ulrich; Cleve, Barbara; Frick, Geneviève
- The Plant Journal, Vol. 12, Issue 3
Chloroplast Phylogenomics Indicates that Ginkgo biloba Is Sister to Cycads
journal, January 2013
- Wu, Chung-Shien; Chaw, Shu-Miaw; Huang, Ya-Yi
- Genome Biology and Evolution, Vol. 5, Issue 1
FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana
journal, October 2001
- Meskauskiene, R.; Nater, M.; Goslings, D.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 22
Tetrapyrrole Biosynthesis in Higher Plants
journal, June 2007
- Tanaka, Ryouichi; Tanaka, Ayumi
- Annual Review of Plant Biology, Vol. 58, Issue 1
Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction
journal, November 2010
- Reinbothe, Christiane; Bakkouri, Majida El; Buhr, Frank
- Trends in Plant Science, Vol. 15, Issue 11
Gene content, organization and molecular evolution of plant organellar genomes and sex chromosomes — Insights from the case of the liverwort Marchantia polymorpha
journal, January 2009
- Ohyama, Kanji; Takemura, Miho; Oda, Kenji
- Proceedings of the Japan Academy, Series B, Vol. 85, Issue 3
Decoding of Light Signals by Plant Phytochromes and Their Interacting Proteins
journal, June 2008
- Bae, Gabyong; Choi, Giltsu
- Annual Review of Plant Biology, Vol. 59, Issue 1
Chloroplast-encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii.
journal, December 1993
- Li, J.; Goldschmidt-Clermont, M.; Timko, M. P.
- The Plant Cell, Vol. 5, Issue 12
Relaxation of Functional Constraint on Light-Independent Protochlorophyllide Oxidoreductase in Thuja
journal, January 2006
- Kusumi, Junko; Sato, Aya; Tachida, Hidenori
- Molecular Biology and Evolution, Vol. 23, Issue 5
Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha
journal, September 2012
- Ueda, Minoru; Kuniyoshi, Tetsuki; Yamamoto, Hiroshi
- The Plant Journal, Vol. 72, Issue 4
DELLAs Regulate Chlorophyll and Carotenoid Biosynthesis to Prevent Photooxidative Damage during Seedling Deetiolation in Arabidopsis
journal, May 2011
- Cheminant, Soizic; Wild, Michael; Bouvier, Florence
- The Plant Cell, Vol. 23, Issue 5
Protochlorophyllide Reduction: Mechanisms and Evolution¶
journal, January 2003
- Schoefs, Benoît; Franck, Fabrice
- Photochemistry and Photobiology, Vol. 78, Issue 6
The evolution of the plastid chromosome in land plants: gene content, gene order, gene function
journal, March 2011
- Wicke, Susann; Schneeweiss, Gerald M.; dePamphilis, Claude W.
- Plant Molecular Biology, Vol. 76, Issue 3-5
Direct transformation of the liverwort Marchantia polymorpha L. by particle bombardment using immature thalli developing from spores
journal, June 2008
- Chiyoda, Shota; Ishizaki, Kimitsune; Kataoka, Hideo
- Plant Cell Reports, Vol. 27, Issue 9
The evolution of the plastid chromosome in land plants: gene content, gene order, gene function
journal, March 2011
- Wicke, Susann; Schneeweiss, Gerald M.; dePamphilis, Claude W.
- Plant Molecular Biology, Vol. 76, Issue 3-5
Simple and efficient plastid transformation system for the liverwort Marchantia polymorpha L. suspension-culture cells
journal, November 2006
- Chiyoda, Shota; Linley, Philip J.; Yamato, Katsuyuki T.
- Transgenic Research, Vol. 16, Issue 1
FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg ++ -branch of this pathway
journal, December 2011
- Kauss, Dominika; Bischof, Sylvain; Steiner, Sandro
- FEBS Letters, Vol. 586, Issue 3
Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction
journal, November 2010
- Reinbothe, Christiane; Bakkouri, Majida El; Buhr, Frank
- Trends in Plant Science, Vol. 15, Issue 11
Evolution of Chlorophyll Biosynthesis—The Challenge to Survive Photooxidation
journal, September 1996
- Reinbothe, Steffen; Reinbothe, Christiane; Apel, Klaus
- Cell, Vol. 86, Issue 5
No single way to understand singlet oxygen signalling in plants
journal, May 2008
- Kim, Chanhong; Meskauskiene, Rasa; Apel, Klaus
- EMBO reports, Vol. 9, Issue 5
Distinct roles for light-dependent NADPH:protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants
journal, April 1996
- Runge, Sonke; Sperling, Ulrich; Frick, Genevieve
- The Plant Journal, Vol. 9, Issue 4
Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns
journal, November 2007
- Jansen, R. K.; Cai, Z.; Raubeson, L. A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
The genomics of symbiosis: Hosts keep the baby and the bath water
journal, September 2002
- Palenik, Brian
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 19
FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana
journal, October 2001
- Meskauskiene, R.; Nater, M.; Goslings, D.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 22
Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I
journal, August 1998
- Shikanai, Toshiharu; Endo, Tsuyoshi; Hashimoto, Takashi
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 16
Chloroplast Phylogenomics Indicates that Ginkgo biloba Is Sister to Cycads
journal, January 2013
- Wu, Chung-Shien; Chaw, Shu-Miaw; Huang, Ya-Yi
- Genome Biology and Evolution, Vol. 5, Issue 1
Identification of the chlB Gene and the Gene Product Essential for the Light-Independent Chlorophyll Biosynthesis in the Cyanobacterium Plectonema boryanum
journal, April 1996
- Fujita, Y.; Takagi, H.; Hase, T.
- Plant and Cell Physiology, Vol. 37, Issue 3
Characterization of cDNA of the Liverwort Phytochrome Gene, and Phytochrome Involvement in the Light-Dependent and Light-Independent Protochlorophyllide Oxidoreductase Gene Expression in Marchantia paleacea var. diptera
journal, June 2001
- Suzuki, Takanori; Takio, Susumu; Yamamoto, Isamu
- Plant and Cell Physiology, Vol. 42, Issue 6
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS
journal, January 1949
- Arnon, Daniel I.
- Plant Physiology, Vol. 24, Issue 1
Rapid Induction of Distinct Stress Responses after the Release of Singlet Oxygen in Arabidopsis
journal, October 2003
- op den Camp, R. G. L.
- THE PLANT CELL ONLINE, Vol. 15, Issue 10
Identification of a Vinyl Reductase Gene for Chlorophyll Synthesis in Arabidopsis thaliana and Implications for the Evolution of Prochlorococcus Species
journal, January 2005
- Nagata, Nozomi; Tanaka, Ryouichi; Satoh, Soichirou
- The Plant Cell, Vol. 17, Issue 1
DELLAs Regulate Chlorophyll and Carotenoid Biosynthesis to Prevent Photooxidative Damage during Seedling Deetiolation in Arabidopsis
journal, May 2011
- Cheminant, Soizic; Wild, Michael; Bouvier, Florence
- The Plant Cell, Vol. 23, Issue 5
Tetrapyrrole Biosynthesis in Higher Plants
journal, June 2007
- Tanaka, Ryouichi; Tanaka, Ayumi
- Annual Review of Plant Biology, Vol. 58, Issue 1
Decoding of Light Signals by Plant Phytochromes and Their Interacting Proteins
journal, June 2008
- Bae, Gabyong; Choi, Giltsu
- Annual Review of Plant Biology, Vol. 59, Issue 1
Light-Independent Chlorophyll Biosynthesis: Involvement of the Chloroplast Gene chlL (frxC)
journal, August 1992
- Suzuki, Jon Y.; Bauer, Carl E.
- The Plant Cell, Vol. 4, Issue 8
Chloroplast-Encoded chlB Is Required for Light-Independent Protochlorophyllide Reductase Activity in Chlamydomonas reinhardtii
journal, December 1993
- Li, Jianming; Goldschmidt-Clermont, Michel; Timko, Michael P.
- The Plant Cell, Vol. 5, Issue 12
Works referencing / citing this record:
The enigmatic loss of light‐independent chlorophyll biosynthesis from an Antarctic green alga in a light‐limited environment
journal, December 2018
- Cvetkovska, Marina; Orgnero, Shane; Hüner, Norman P. A.
- New Phytologist, Vol. 222, Issue 2
Dark chlorophyll synthesis may provide a potential for shade tolerance as shown by a comparative study with seedlings of European larch (Larix decidua) and Norway spruce (Picea abies)
journal, March 2018
- Stolárik, Tibor; Nožková, Vladimíra; Nosek, Lukáš
- Trees, Vol. 32, Issue 4
The Effect of Two Amino acid Residue Substitutions via RNA Editing on Dark-operative Protochlorophyllide Oxidoreductase in the Black Pine Chloroplasts
journal, May 2017
- Yamamoto, Haruki; Kusumi, Junko; Yamakawa, Hisanori
- Scientific Reports, Vol. 7, Issue 1
A Cyan Fluorescent Reporter Expressed from the Chloroplast Genome of Marchantia polymorpha.
journalarticle, January 2016
- Boehm, Christian R.; Ueda, Minoru; Nishimura, Yoshiki
- Oxford University Press (OUP)
Impaired Magnesium Protoporphyrin IX Methyltransferase (ChlM) Impedes Chlorophyll Synthesis and Plant Growth in Rice
journal, September 2017
- Wang, Zhaohai; Hong, Xiao; Hu, Keke
- Frontiers in Plant Science, Vol. 8