title: Marine algae and land plants share conserved phytochrome signaling systems.
abstract: Phytochrome photosensors control a vast gene network in streptophyte plants, acting as master regulators of diverse growth and developmental processes throughout the life cycle. In contrast with their absence in known chlorophyte algal genomes and most sequenced prasinophyte algal genomes, a phytochrome is found in Micromonas pusilla, a widely distributed marine picoprasinophyte (<2 µm cell diameter). Together with phytochromes identified from other prasinophyte lineages, we establish that prasinophyte and streptophyte phytochromes share core light-input and signaling-output domain architectures except for the loss of C-terminal response regulator receiver domains in the streptophyte phytochrome lineage. Phylogenetic reconstructions robustly support the presence of phytochrome in the common progenitor of green algae and land plants. These analyses reveal a monophyletic clade containing streptophyte, prasinophyte, cryptophyte, and glaucophyte phytochromes implying an origin in the eukaryotic ancestor of the Archaeplastida. Transcriptomic measurements reveal diurnal regulation of phytochrome and bilin chromophore biosynthetic genes in Micromonas. Expression of these genes precedes both light-mediated phytochrome redistribution from the cytoplasm to the nucleus and increased expression of photosynthesis-associated genes. Prasinophyte phytochromes perceive wavelengths of light transmitted farther through seawater than the red/far-red light sensed by land plant phytochromes. Prasinophyte phytochromes also retain light-regulated histidine kinase activity lost in the streptophyte phytochrome lineage. Our studies demonstrate that light-mediated nuclear translocation of phytochrome predates the emergence of land plants and likely represents a widespread signaling mechanism in unicellular algae.
authors.affiliation: Department of Molecular and Cellular Biology, University of California, Davis, CA 95616;
authors.forename: Deqiang
authors.initials: D
authors.lastname: Duanmu
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
authors.forename: Charles
authors.initials: C
authors.lastname: Bachy
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
authors.forename: Sebastian
authors.initials: S
authors.lastname: Sudek
authors.affiliation: Sequencing Technology Group, Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, CA 94598;
authors.forename: Chee-Hong
authors.initials: CH
authors.lastname: Wong
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
authors.forename: Valeria
authors.initials: V
authors.lastname: Jiménez
authors.affiliation: Department of Molecular and Cellular Biology, University of California, Davis, CA 95616;
authors.forename: Nathan C
authors.initials: NC
authors.lastname: Rockwell
authors.affiliation: Department of Molecular and Cellular Biology, University of California, Davis, CA 95616;
authors.forename: Shelley S
authors.initials: SS
authors.lastname: Martin
authors.affiliation: Sequencing Technology Group, Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, CA 94598;
authors.forename: Chew Yee
authors.initials: CY
authors.lastname: Ngan
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
authors.forename: Emily N
authors.initials: EN
authors.lastname: Reistetter
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
authors.forename: Marijke J
authors.initials: MJ
authors.lastname: van Baren
authors.affiliation: Department of Ecology, Evolution, and Natural Resources, Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ 08903;
authors.forename: Dana C
authors.initials: DC
authors.lastname: Price
authors.affiliation: Sequencing Technology Group, Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, CA 94598;
authors.forename: Chia-Lin
authors.initials: CL
authors.lastname: Wei
authors.affiliation: Biology Department, University of New Brunswick, Fredericton, NB, Canada E3B5A3; and Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8.
authors.forename: Adrian
authors.initials: A
authors.lastname: Reyes-Prieto
authors.affiliation: Department of Molecular and Cellular Biology, University of California, Davis, CA 95616; jclagarias@ucdavis.edu azworden@mbari.org.
authors.forename: J Clark
authors.initials: JC
authors.lastname: Lagarias
authors.affiliation: Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039; Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8 jclagarias@ucdavis.edu azworden@mbari.org.
authors.forename: Alexandra Z
authors.initials: AZ
authors.lastname: Worden
mesh_terms: D059001:Aquatic Organisms / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D001483:Base Sequence; D002467:Cell Nucleus / Q000235:genetics / Q000378:metabolism; D000460:Chlorophyta / Q000235:genetics / Q000378:metabolism; D003593:Cytoplasm / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D008969:Molecular Sequence Data; D010802:Phylogeny; D010834:Phytochrome / Q000096:biosynthesis / Q000235:genetics; D017434:Protein Structure, Tertiary; D015398:Signal Transduction / Q000502:physiology*; D059467:Transcriptome / Q000502:physiology
chemical_list: D010834:Phytochrome
keywords: light harvesting; light signaling evolution; marine ecology; phytoplankton; transcriptomics