Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

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

doi:10.1105/tpc.17.00149

Title: Bilin-Dependent Photoacclimation in Chlamydomonas reinhardtii

Journal Article · Mon Oct 30 00:00:00 EDT 2017 · The Plant Cell

DOI:https://doi.org/10.1105/tpc.17.00149· OSTI ID:1405560

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Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305, Department of Biology, Stanford University, Stanford, California 94305
Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90095, Institute for Genomics and Proteomics, University of California, Los Angeles, California 90095
Department of Plant Biology, Carnegie Institution for Science, Stanford, California 94305
Department of Molecular and Cellular Biology, University of California, Davis, California 95616
College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China
Department of Chemistry and Biochemistry, University of California, Los Angeles, California 90095
Horticultural Sciences Department, University of Florida, Gainesville, Florida 32611
Department of Molecular and Cellular Biology, University of California, Davis, California 95616, State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan 430070, China

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.

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