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Title: Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

Abstract

In land plants, linear tetrapyrrole (bilin)-based phytochrome photosensors optimize photosynthetic light capture by mediating massive reprogramming of gene expression. But, surprisingly, many green algal genomes lack phytochrome genes. Studies of the heme oxygenase mutant ( hmox1) of the green alga Chlamydomonas reinhardtii suggest that bilin biosynthesis in plastids is essential for proper regulation of a nuclear gene network implicated in oxygen detoxification during dark-to-light transitions. hmox1 cannot grow photoautotrophically and photoacclimates poorly to increased illumination. We show that these phenotypes are due to reduced accumulation of photosystem I (PSI) reaction centers, the PSI electron acceptors 5'-monohydroxyphylloquinone and phylloquinone, and the loss of PSI and photosystem II antennae complexes during photoacclimation. The hmox1 mutant resembles chlorophyll biosynthesis mutants phenotypically, but can be rescued by exogenous biliverdin IXα, the bilin produced by HMOX1. This rescue is independent of photosynthesis and is strongly dependent on blue light. RNA-seq comparisons of hmox1, genetically complemented hmox1, and chemically rescued hmox1 reveal that tetrapyrrole biosynthesis and known photoreceptor and photosynthesis-related genes are not impacted in the hmox1 mutant at the transcript level. We propose that a bilin-based, blue-light-sensing system within plastids evolved together with a bilin-based retrograde signaling pathway to ensure that a robust photosynthetic apparatusmore » is sustained in light-grown Chlamydomonas.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [5]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [6];  [6]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [7]; ORCiD logo [4]
  1. Stanford Univ., CA (United States); Carnegie Inst. of Science, Stanford, CA (United States); Salk Inst. for Biological Studies, La Jolla, CA (United States)
  2. Univ. of California, Los Angeles, CA (United States)
  3. Carnegie Inst. of Science, Stanford, CA (United States)
  4. Univ. of California, Davis, CA (United States)
  5. Huazhong Agricultural Univ., Wuhan (China)
  6. Univ. of Florida, Gainesville, FL (United States)
  7. Univ. of California, Davis, CA (United States); Huazhong Agricultural Univ., Wuhan (China)
Publication Date:
Research Org.:
Univ. of California, Los Angeles, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1405560
Alternate Identifier(s):
OSTI ID: 1511837
Grant/Contract Number:  
FG02-04ER15529
Resource Type:
Journal Article: Published Article
Journal Name:
Plant Cell
Additional Journal Information:
Journal Volume: 29; Journal Issue: 11; Journal ID: ISSN 1040-4651
Publisher:
American Society of Plant Biologists
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Wittkopp, Tyler M., Schmollinger, Stefan, Saroussi, Shai, Hu, Wei, Zhang, Weiqing, Fan, Qiuling, Gallaher, Sean D., Leonard, Michael T., Soubeyrand, Eric, Basset, Gilles J., Merchant, Sabeeha S., Grossman, Arthur R., Duanmu, Deqiang, and Lagarias, J. Clark. Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii. United States: N. p., 2017. Web. doi:10.1105/tpc.17.00149.
Wittkopp, Tyler M., Schmollinger, Stefan, Saroussi, Shai, Hu, Wei, Zhang, Weiqing, Fan, Qiuling, Gallaher, Sean D., Leonard, Michael T., Soubeyrand, Eric, Basset, Gilles J., Merchant, Sabeeha S., Grossman, Arthur R., Duanmu, Deqiang, & Lagarias, J. Clark. Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii. United States. doi:10.1105/tpc.17.00149.
Wittkopp, Tyler M., Schmollinger, Stefan, Saroussi, Shai, Hu, Wei, Zhang, Weiqing, Fan, Qiuling, Gallaher, Sean D., Leonard, Michael T., Soubeyrand, Eric, Basset, Gilles J., Merchant, Sabeeha S., Grossman, Arthur R., Duanmu, Deqiang, and Lagarias, J. Clark. Wed . "Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii". United States. doi:10.1105/tpc.17.00149.
@article{osti_1405560,
title = {Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii},
author = {Wittkopp, Tyler M. and Schmollinger, Stefan and Saroussi, Shai and Hu, Wei and Zhang, Weiqing and Fan, Qiuling and Gallaher, Sean D. and Leonard, Michael T. and Soubeyrand, Eric and Basset, Gilles J. and Merchant, Sabeeha S. and Grossman, Arthur R. and Duanmu, Deqiang and Lagarias, J. Clark},
abstractNote = {In land plants, linear tetrapyrrole (bilin)-based phytochrome photosensors optimize photosynthetic light capture by mediating massive reprogramming of gene expression. But, surprisingly, many green algal genomes lack phytochrome genes. Studies of the heme oxygenase mutant (hmox1) of the green alga Chlamydomonas reinhardtii suggest that bilin biosynthesis in plastids is essential for proper regulation of a nuclear gene network implicated in oxygen detoxification during dark-to-light transitions. hmox1 cannot grow photoautotrophically and photoacclimates poorly to increased illumination. We show that these phenotypes are due to reduced accumulation of photosystem I (PSI) reaction centers, the PSI electron acceptors 5'-monohydroxyphylloquinone and phylloquinone, and the loss of PSI and photosystem II antennae complexes during photoacclimation. The hmox1 mutant resembles chlorophyll biosynthesis mutants phenotypically, but can be rescued by exogenous biliverdin IXα, the bilin produced by HMOX1. This rescue is independent of photosynthesis and is strongly dependent on blue light. RNA-seq comparisons of hmox1, genetically complemented hmox1, and chemically rescued hmox1 reveal that tetrapyrrole biosynthesis and known photoreceptor and photosynthesis-related genes are not impacted in the hmox1 mutant at the transcript level. We propose that a bilin-based, blue-light-sensing system within plastids evolved together with a bilin-based retrograde signaling pathway to ensure that a robust photosynthetic apparatus is sustained in light-grown Chlamydomonas.},
doi = {10.1105/tpc.17.00149},
journal = {Plant Cell},
issn = {1040-4651},
number = 11,
volume = 29,
place = {United States},
year = {2017},
month = {11}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1105/tpc.17.00149

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Cited by: 5 works
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