title: The regulation of photosynthetic structure and function during nitrogen deprivation in Chlamydomonas reinhardtii.
abstract: The accumulation of carbon storage compounds by many unicellular algae after nutrient deprivation occurs despite declines in their photosynthetic apparatus. To understand the regulation and roles of photosynthesis during this potentially bioenergetically valuable process, we analyzed photosynthetic structure and function after nitrogen deprivation in the model alga Chlamydomonas reinhardtii. Transcriptomic, proteomic, metabolite, and lipid profiling and microscopic time course data were combined with multiple measures of photosynthetic function. Levels of transcripts and proteins of photosystems I and II and most antenna genes fell with differing trajectories; thylakoid membrane lipid levels decreased, while their proportions remained similar and thylakoid membrane organization appeared to be preserved. Cellular chlorophyll (Chl) content decreased more than 2-fold within 24 h, and we conclude from transcript protein and (13)C labeling rates that Chl synthesis was down-regulated both pre- and posttranslationally and that Chl levels fell because of a rapid cessation in synthesis and dilution by cellular growth rather than because of degradation. Photosynthetically driven oxygen production and the efficiency of photosystem II as well as P700(+) reduction and electrochromic shift kinetics all decreased over the time course, without evidence of substantial energy overflow. The results also indicate that linear electron flow fell approximately 15% more than cyclic flow over the first 24 h. Comparing Calvin-Benson cycle transcript and enzyme levels with changes in photosynthetic (13)CO2 incorporation rates also pointed to a coordinated multilevel down-regulation of photosynthetic fluxes during starch synthesis before the induction of high triacylglycerol accumulation rates.
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Matthew T
authors.initials: MT
authors.lastname: Juergens
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Rahul R
authors.initials: RR
authors.lastname: Deshpande
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Ben F
authors.initials: BF
authors.lastname: Lucker
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Jeong-Jin
authors.initials: JJ
authors.lastname: Park
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Hongxia
authors.initials: H
authors.lastname: Wang
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Mahmoud
authors.initials: M
authors.lastname: Gargouri
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: F Omar
authors.initials: FO
authors.lastname: Holguin
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Bradley
authors.initials: B
authors.lastname: Disbrow
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Tanner
authors.initials: T
authors.lastname: Schaub
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Jeremy N
authors.initials: JN
authors.lastname: Skepper
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: David M
authors.initials: DM
authors.lastname: Kramer
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: David R
authors.initials: DR
authors.lastname: Gang
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.).
authors.forename: Leslie M
authors.initials: LM
authors.lastname: Hicks
authors.affiliation: Department of Plant Biology (M.T.J., R.R.D., B.D., Y.S.-H.) and Plant Research Laboratory (M.T.J., B.F.L., D.M.K.), Michigan State University, East Lansing, Michigan 48824;Institute of Biological Chemistry, Washington State University, Pullman, Washington 99164 (J.-J.P., M.G., D.R.G.);Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (H.W., L.M.H.);National Center of Biomedical Analysis, Beijing 100850, China (H.W.);College of Agricultural, Consumer, and Environmental Sciences, New Mexico State University, Las Cruces, New Mexico 88003 (F.O.H., T.S.);Department of Physiology, Cambridge Advanced Imaging Centre, Cambridge CB2 3DY, United Kingdom (J.N.S.); andDepartment of Chemistry, University of North Carolina, Chapel Hill, North Carolina 27599 (L.M.H.) yairhill@msu.edu.
authors.forename: Yair
authors.initials: Y
authors.lastname: Shachar-Hill
mesh_terms: D057486:Carbon Cycle; D002247:Carbon Isotopes; D016825:Chlamydomonas reinhardtii / Q000235:genetics / Q000502:physiology* / Q000648:ultrastructure; D002734:Chlorophyll / Q000378:metabolism; D015536:Down-Regulation / Q000235:genetics; D004734:Energy Metabolism; D005453:Fluorescence; D018506:Gene Expression Regulation, Plant; D008055:Lipids / Q000032:analysis; D009584:Nitrogen / Q000172:deficiency*; D010100:Oxygen / Q000378:metabolism; D010788:Photosynthesis; D045331:Photosystem I Protein Complex / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D018892:Proton-Motive Force; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D013213:Starch / Q000096:biosynthesis; D020524:Thylakoids / Q000378:metabolism / Q000648:ultrastructure
chemical_list: D002247:Carbon Isotopes; D008055:Lipids; D045331:Photosystem I Protein Complex; D010940:Plant Proteins; D012333:RNA, Messenger; D002734:Chlorophyll; D013213:Starch; D009584:Nitrogen; D010100:Oxygen