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Novel Metabolism in Chlamydomonas Through the Lens of Genomics Arthur R Genetics, Development and Cell Biology Genetics, Development and Cell Biology Publications 4-2007 Novel metabolism in Chlamydomonas through the lens of genomics Arthur R. Grossman The Carnegie Institution Martin Croft University of Cambridge Vadim N. Gladyshev University of Nebraska - Lincoln Sabeeha Merchant University of California, Los Angeles Matthew .C Posewitz Colorado School of Mines See next page for additional authors Follow this and additional works at: http://lib.dr.iastate.edu/gdcb_las_pubs Part of the Genetics and Genomics Commons, and the Plant Breeding and Genetics Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ gdcb_las_pubs/176. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Genetics, Development and Cell Biology at Iowa State University Digital Repository. It has been accepted for inclusion in Genetics, Development and Cell Biology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Novel metabolism in Chlamydomonas through the lens of genomics Abstract Chlamydomonas has traditionally been exploited as an organism that is associated with sophisticated physiological, genetic and molecular analyses, all of which have been used to elucidate several biological processes, especially photosynthesis and flagella function and assembly. Recently, the genomics of Chlamydomonas has been combined with other technologies to unveil new aspects of metabolism, including inorganic carbon utilization, anaerobic fermentation, the suite and functions of selenoproteins, and the regulation of vitamin biosynthesis. These initial findings represent the first glimpse through a genomic window onto the highly complex metabolisms that characterize a unicellular, photosynthetic eukaryote that has maintained both plant-like and animal-like characteristics over evolutionary time. Disciplines Genetics and Genomics | Plant Breeding and Genetics Comments This article is published as Grossman, Arthur R., Martin Croft, Vadim N. Gladyshev, Sabeeha S. Merchant, Matthew C. Posewitz, Simon Prochnik, and Martin H. Spalding. "Novel metabolism in Chlamydomonas through the lens of genomics." Current opinion in plant biology 10, no. 2 (2007): 190-198. 10.1016/ j.pbi.2007.01.012. Posted with permission. Rights Works produce by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The onc tent of this document is not copyrighted. Authors Arthur R. Grossman, Martin Croft, Vadim N. Gladyshev, Sabeeha Merchant, Matthew C. Posewitz, Simon Prochnik, and Martin H. Spalding This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/gdcb_las_pubs/176 Novel metabolism in Chlamydomonas through the lens of genomics Arthur R Grossman1, Martin Croft2, Vadim N Gladyshev3, Sabeeha S Merchant4, Matthew C Posewitz5, Simon Prochnik6 and Martin H Spalding7 Chlamydomonas has traditionally been exploited as an eukaryotic chloroplast biology and the biogenesis and organism that is associated with sophisticated physiological, action of flagella and basal bodies [1–3]. Genetic analyses genetic and molecular analyses, all of which have been used to with this organism began in the mid 20th century and elucidate several biological processes, especially developed into sophisticated molecular and genomic photosynthesis and flagella function and assembly. Recently, technologies for dissecting biological processes. Unique the genomics of Chlamydomonas has been combined with attributes that make Chlamydomonas ideal for dissecting other technologies to unveil new aspects of metabolism, photosynthesis are its ability to grow heterotrophically in including inorganic carbon utilization, anaerobic fermentation, the dark by metabolizing exogenous acetate, and its the suite and functions of selenoproteins, and the regulation of maintenance of a normal green chloroplast that retains vitamin biosynthesis. These initial findings represent the first the capacity to perform oxygenic photosynthesis when glimpse through a genomic window onto the highly complex illuminated following growth in the dark. These charac- metabolisms that characterize a unicellular, photosynthetic teristics have allowed the isolation of a range of mutants in eukaryote that has maintained both plant-like and animal-like which the function and biogenesis of the photosynthetic characteristics over evolutionary time. apparatus is adversely affected [1,4]. Most other photo- Addresses synthetic organisms and all vascular plants either do not 1 Department of Plant Biology, The Carnegie Institution, 260 Panama survive or exhibit growth retardation and pigment loss in Street, Stanford, California 94305, USA the absence of photosynthesis. Recent work on photo- 2 Department of Plant Sciences, University of Cambridge, Downing synthesis in Chlamydomonas has focused on the discovery Street, Cambridge, UK 3 Department of Biochemistry, N151 Beadle Center, University of of molecules that catalyze the assembly of the photosyn- Nebraska, Lincoln, Nebraska 68588-0664, USA thetic apparatus and determine the abundance and rate of 4 Department of Chemistry & Biochemistry, UCLA, Box 951569, synthesis of individual complexes, and regulatory mol- Los Angeles, California 90095-1569, USA ecules that control the distribution of excitation energy 5 Environmental Science & Engineering Division, Colorado School of Mines, Golden, Colorado 80401, USA (state transitions) or dissipation of excess absorbed light 6 DOE Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, energy (non-photochemical quenching) [2,5,6]. California 94598, USA 7 Department of Genetics, Development and Cell Biology, 1210 Many molecular technologies have also been applied to Molecular Biology, Iowa State University, Ames, Iowa 50011-3260, USA studies of Chlamydomonas. The chloroplast and nuclear Corresponding author: Grossman, Arthur R ([email protected]) genomes of this alga are readily transformed [7]. Plasmid, cosmid, and bacterial artificial chromosome (BAC) libraries are available. Methods have been developed to Current Opinion in Plant Biology 2007, 10:190–198 generate and identify tagged mutant alleles. Alleles that This review comes from a themed issue on are not tagged can be identified by map-based cloning Genome studies and molecular genetics [8,9 ]. Gene function can be evaluated by suppression of Edited by Stefan Jansson and Edward S Buckler specific gene activities using antisense or RNA interfer- ence (RNAi) constructs [10], and reporter genes have been Available online 8th February 2007 developed to identify regulatory factors and sequences 1369-5266/$ – see front matter that are involved in regulating gene expression [11]. # 2006 Elsevier Ltd. All rights reserved. In this review, we discuss how the genomics of Chlamy- DOI 10.1016/j.pbi.2007.01.012 domonas are being combined with these other technol- ogies to unveil new aspects of metabolism, including inorganic carbon utilization, anaerobic fermentation, Introduction the suite and functions of selenoproteins, and the regu- Chlamydomonas reinhardtii is a member of the green algal lation of vitamin biosynthesis. The facts and concepts lineage that diverged from the streptophytes approxi- discussed below represent initial insights into the highly mately one billion years ago. It has served as an out- complex metabolisms that characterize a unicellular, standing model organism, especially for analyzing photosynthetic eukaryote. Current Opinion in Plant Biology 2007, 10:190–198 www.sciencedirect.com Novel metabolism in Chlamydomonas Grossman et al. 191 Current status of the genome and genome Box 1 Genome-associated resources for Chlamydomonas. resources JGI Chlamydomonas Genome Portal: http://genome.jgi-psf.org/ The value of the technologies described above is aug- Chlre3/Chlre3.home.html mented by the nearly 300 000 expressed sequence tags cDNA libraries: http://www.chlamy.org/libraries.html (and the (ESTs) [12,13 ,14] and a draft Chlamydomonas genome associated sites) sequence (http://genome.jgi-psf.org/Chlre3/Chlre3. Kazusa EST database: http://www.kazusa.or.jp/en/plant/chlamy/ home.html). Several different Chlamydomonas cDNA EST/ libraries were constructed using RNA from cells grown BAC libraries: http://www.genome.clemson.edu under different environmental conditions (see Table 1; [12]). The EST sequences were assembled on the basis of BAC end sequences: http://genome.jgi-psf.org/cgi-bin/ sequence similarity, paired-end sequence information, getPlateSeq?db=chlre2andprefix=PTQanddatalib=chlre_bacends and genomic information to generate a set of Unigenes Flagellar proteome: http://laboratories.umassmed.edu/chlamyfp/ designated ACEGs (for ‘Assembly of Contiguous ESTs index.php verified by Genome sequences’) (M Jain et al., unpub- Genome annotation: http://www.chlamydomonas.info/ lished). Unigene sets were used to develop both cDNA- and oligonucleotide (70mer)-based microarrays [13,15]. The current draft release (version 3.0) of the C. reinhardtii allowing high rates of photosynthetic CO2 fixation when genome (a detailed description to be published elsewhere), the concentration of external Ci (where Ci is CO2, À À2 generated at the Joint Genome Institute (JGI), used geno- HCO3 and CO3 ) is low. A CCM is crucial for Chla- mic DNA from strain CC-503 cw92 mt+. A whole-genome
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