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First published online October 6, 2006; 10.1104/pp.106.086090 Plant Physiology 142:911-922 (2006) © 2006 American Society of Plant Biologists Differential Operation of Dual Protochlorophyllide Reductases for Chlorophyll Biosynthesis in Response to Environmental Oxygen Levels in the Cyanobacterium Leptolyngbya boryana1Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 4648601, Japan
Most oxygenic phototrophs, including cyanobacteria, have two structurally unrelated protochlorophyllide (Pchlide) reductases in the penultimate step of chlorophyll biosynthesis. One is light-dependent Pchlide reductase (LPOR) and the other is dark-operative Pchlide reductase (DPOR), a nitrogenase-like enzyme assumed to be sensitive to oxygen. Very few studies have been conducted on how oxygen-sensitive DPOR operates in oxygenic phototrophic cells. Here, we report that anaerobic conditions are required for DPOR to compensate for the loss of LPOR in cyanobacterial cells. An LPOR-lacking mutant of the cyanobacterium Leptolyngbya boryana (formerly Plectonema boryanum) failed to grow in high light conditions and this phenotype was overcome by cultivating it under anaerobic conditions (2% CO2/N2). The critical oxygen level enabling the mutant to grow in high light was determined to be 3% (v/v). Oxygen-sensitive Pchlide reduction activity was successfully detected as DPOR activity in cell-free extracts of anaerobically grown mutants, whereas activity was undetectable in the wild type. The content of two DPOR subunits, ChlL and ChlN, was significantly increased in mutant cells compared with wild type. This suggests that the increase in subunits stimulates the DPOR activity that is protected efficiently from oxygen by anaerobic environments, resulting in complementation of the loss of LPOR. These results provide important concepts for understanding how dual Pchlide reductases operate differentially in oxygenic photosynthetic cells grown under natural environments where oxygen levels undergo dynamic changes. The evolutionary implications of the coexistence of two Pchlide reductases are discussed.
1 This work was supported by Grants-in-Aid for Scientific Research (grant nos. 13740456, 15570033, 14390051, 13CE2005, and 14COEA2 to Y.F.) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Yuichi Fujita (fujita{at}agr.nagoya-u.ac.jp). www.plantphysiol.org/cgi/doi/10.1104/pp.106.086090 * Corresponding author; e-mail fujita{at}agr.nagoya-u.ac.jp; fax 81527894107. Received June 30, 2006; accepted September 14, 2006; published October 6, 2006. This article has been cited by other articles:
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