期刊论文详细信息
BMC Evolutionary Biology
A novel type of light-harvesting antenna protein of red algal origin in algae with secondary plastids
Johann Lavaud3  Iwona Adamska2  Peter G Kroth5  Sascha Vugrinec5  Ansgar Gruber4  Johannes Engelken1  Sabine Sturm5 
[1] Present address: Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), 08003 Barcelona,Spain;Biochemie und Physiologie der Pflanzen, Fach 602, Universität Konstanz 78457 Konstanz, Germany;Present address: UMR 7266 CNRS-ULR ’LIENSs’, CNRS/University of La Rochelle, Institute for Coastal and Environmental Research, La Rochelle Cedex, France;Present address: Department of Biochemistry & Molecular Biology, Dalhousie University, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, Nova Scotia B3H 4R2, Canada;Ökophysiologie der Pflanzen, Fach 611, Universität Konstanz 78457 Konstanz, Germany
关键词: Red lineage chlorophyll a/b-binding-like proteins;    Light-harvesting antenna proteins;    Gene transfer;    Chloroplast;    Diatoms;    Complex plastids;   
Others  :  1086737
DOI  :  10.1186/1471-2148-13-159
 received in 2013-01-30, accepted in 2013-07-22,  发布年份 2013
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【 摘 要 】

Background

Light, the driving force of photosynthesis, can be harmful when present in excess; therefore, any light harvesting system requires photoprotection. Members of the extended light-harvesting complex (LHC) protein superfamily are involved in light harvesting as well as in photoprotection and are found in the red and green plant lineages, with a complex distribution pattern of subfamilies in the different algal lineages.

Results

Here, we demonstrate that the recently discovered “red lineage chlorophyll a/b-binding-like proteins” (RedCAPs) form a monophyletic family within this protein superfamily. The occurrence of RedCAPs was found to be restricted to the red algal lineage, including red algae (with primary plastids) as well as cryptophytes, haptophytes and heterokontophytes (with secondary plastids of red algal origin). Expression of a full-length RedCAP:GFP fusion construct in the diatom Phaeodactylum tricornutum confirmed the predicted plastid localisation of RedCAPs. Furthermore, we observed that similarly to the fucoxanthin chlorophyll a/c-binding light-harvesting antenna proteins also RedCAP transcripts in diatoms were regulated in a diurnal way at standard light conditions and strongly repressed at high light intensities.

Conclusions

The absence of RedCAPs from the green lineage implies that RedCAPs evolved in the red lineage after separation from the the green lineage. During the evolution of secondary plastids, RedCAP genes therefore must have been transferred from the nucleus of the endocytobiotic alga to the nucleus of the host cell, a process that involved complementation with pre-sequences allowing import of the gene product into the secondary plastid bound by four membranes. Based on light-dependent transcription and on localisation data, we propose that RedCAPs might participate in the light (intensity and quality)-dependent structural or functional reorganisation of the light-harvesting antennae of the photosystems upon dark to light shifts as regularly experienced by diatoms in nature. Remarkably, in plastids of the red lineage as well as in green lineage plastids, the phycobilisome based cyanobacterial light harvesting system has been replaced by light harvesting systems that are based on members of the extended LHC protein superfamily, either for one of the photosystems (PS I of red algae) or for both (diatoms). In their proposed function, the RedCAP protein family may thus have played a role in the evolutionary structural remodelling of light-harvesting antennae in the red lineage.

【 授权许可】

   
2013 Sturm et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Montané MH, Kloppstech K: The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 2000, 258:1-8.
  • [2]Li Z, Wakao S, Fischer BB, Niyogi KK: Sensing and responding to excess light. Ann Rev Plant Biol 2009, 60:239-260.
  • [3]Ballottari M, Girardon J, Dall’osto L, Bassi R: Evolution and functional properties of photosystem II light-harvesting complexes in eukaryotes. Biochim Biophys Acta 2011, 1817:143-157.
  • [4]Jansson S: A protein family saga: From photoprotection to light harvesting (and back?). In Photoprotection, Photoinhibition, Gene Regulation, and Environment Volume 21. Edited by K MA, Demmig-Adams B, Demmig-Adams B, Adams WWr, K MA. The Netherlands: Springer; 2006:145-153.
  • [5]Green BR: Evolution of light-harvesting antennas in an oxygen world. In Evolution of Primary Producers in the Sea. Edited by Falkowski PG, Falkowski PG, Knoll AH. Burlington: Elsevier Academic Press; 2007:37-53.
  • [6]Koziol AG, Borza T, Ishida KI, Keeling P, Lee RW, Durnford DE: Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 2007, 143:1802-1816.
  • [7]Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK: An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 2009, 462:518-522.
  • [8]Neilson JA, Durnford DG: Evolutionary distribution of light-harvesting complex-like protein in photosynthetic eukaryots. Genome 2010, 53:68-78.
  • [9]Engelken J, Funk C, Adamska I: The extended light-harvesting complex (LHC) protein superfamily: Classification and evolutionary dynamics. In Functional Genomics and Evolution of Photosynthetic Systems, Volume 33. Edited by Burnap RL, Vermaas WFJ. Dordrecht: Springer Science+Buisness Media, B.V; 2012:265-284. [Advances in Photosynthesis and Respiration, vol 33]
  • [10]Wolfe GR, Cunningham FX, Durnford D, Green BR, Gantt E: Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 1994, 367:566-568.
  • [11]Engelken J, Brinkmann H, Adamska I: Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol Biol 2010, 10:223. BioMed Central Full Text
  • [12]La Roche J, van der Staay GWM, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AWD, Green BR: Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci 1996, 93(26):15244-15248.
  • [13]Yeremenko N, Kouřil R, Ihalainen JA, D’Haene S, van Oosterwijk N, Andrizhiyevskaya EG, Keegstra W, Dekker HL, Hagemann M, Boekema EJ, Matthijs HCP, Dekker JP: Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 2004, 43(32):10308-10313.
  • [14]Keeling PJ: The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc B: Biol Sci 2010, 365:729-748.
  • [15]Green BR: After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res 2011, 107:103-115.
  • [16]Dorrell RG, Smith AG: Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates. Eukaryot Cell 2011, 10:856-868.
  • [17]Cavalier-Smith T: Chloroplast evolution: secondary symbiogenesis and multiple losses. Current Biol 2002, 12:R62-R64.
  • [18]Hoffman GE, Sanchez Puerta MV, Delwiche CF: Evolution of light-harvesting complex proteins from Chl c-containing algae. BMC Evol Biol 2011, 11:101. BioMed Central Full Text
  • [19]Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, Niyogi KK, Bassi R: Analysis of LhcSR3, a protein essential for feedback de-excitation in the green Alga Chlamydomonas reinhardtii. PLoS Biol 2011, 9:e1000577.
  • [20]Heddad M, Engelken J, Adamska I: Light stress proteins in viruses, cyanobacteria and photosynthetic eukaryotes. In Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation. Edited by Tripathy BC, Eaton-Rye JJ, Tripathy BC, Sharkey TD. Dordrecht: Springer Science+Buisness Media, B.V; 2012:299-317. [Advances in Photosynthesis and Respiration, vol 34]
  • [21]Dittami SM, Scornet D, Petit JL, Ségurens B, Silva CD, Corre E, Dondrup M, Glatting KH, König R, Sterck L, Rouzé P, de Peer YV, Cock JM, Boyen C, Tonon T: Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol 2009, 10:R66. BioMed Central Full Text
  • [22]Online Resource for Community Annotation of Eukaryotes Ectocarpus siliculosus http://bioinformatics.psb.ugent.be/orcae/overview/Ectsi webcite
  • [23]Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, Amoutzias G, Anthouard V, Artiguenave F, Aury JM, Badger JH, Beszteri B, Billiau K, Bonnet E, Bothwell JH, Bowler C, Boyen C, Brownlee C, Carrano CJ, Charrier B, Cho GY, Coelho SM, Collén J, Corre E, Silva CD, Delage L, Delaroque N, Dittami SM, Doulbeau S, Elias M, Farnham G, et al.: The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 2010, 465(7298):617-621.
  • [24]Dittami SM, Riisberg I, John U, Orr RJ, Jakobsen KS, Edvardsen B: Analysis of expressed sequence tags from the marine microalga Pseudochattonella farcimen (Dictyochophyceae). Protist 2012, 163:143-161.
  • [25]Gobler CJ, Berry DL, Dyhrman ST, Wilhelm SW, Salamov A, Lobanov AV, Zhang Y, Collier JL, Wurch LL, Kustka AB, Dill BD, Shah M, VerBerkmoes NC, Kuo A, Terry A, Pangilinan J, Lindquist EA, Lucas S, Paulsen IT, Hattenrath-Lehmann TK, Talmage SC, Walker EA, Koch F, Burson AM, Marcoval MA, Tang YZ, LeCleir GR, Coyne KJ, Berg GM, Bertrand EM, et al.: Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci 2011, 108:4352-4357.
  • [26]Kostamo K, Olsson S, Korpelainen H: Search for stress-responsive genes in the red alga Furcellaria lumbricalis (Rhodophyta) by expressed sequence tag analysis. J Exp Mar Biol Ecol 2011, 404:21-25.
  • [27]Lee H, Lee HK, An G, Lee YK: Analysis of expressed sequence tags from the red alga Griffithsia okiensis. J Microbiol 2007, 45:541-54.
  • [28]Nikaido I, Asamizu E, Nakajima M, Nakamura Y, Saga N, Tabata S: Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res 2000, 7:223-227.
  • [29]Chan CX, Yang EC, Banerjee T, Yoon HS, Martone PT, Estevez JM, Bhattacharya D: Red and green algal monophyly and extensive gene sharing found in a rich repertoire of red algal genes. Curr Biol 2011, 21:328-333.
  • [30]Matsuzaki M, Misumi O, Shin-i T, Maruyama S, Takahara M, Miyagishima Sy, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y: Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 2004, 428(6983):653-657.
  • [31]Kilian O, Soisig Steunou A, Grossman AR, Bhaya D: A novel two-domain fusion protein in cyanobacteria with similarity to the CAB/ELIP/HLIP superfamily: Evolutionary implications and regulation. Mol Plant 2008, 1:155-166.
  • [32]Kilian O, Kroth PG: Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 2005, 41:175-183.
  • [33]Gruber A, Vugrinec S, Hempel F, Gould SB, Maier UG, Kroth PG: Protein targeting into complex diatom plastids: functional characterization of a specific targeting motif. Plant Mol Biol 2007, 64:519-530.
  • [34]Patron NJ, Waller RF: Transit peptide diversity and divergence: A global analysis of plastid targeting signals. BioEssays 2007, 29:1048-1058.
  • [35]Kilian O, Kroth PG: Presequence acquisition during secondary endocytobiosis and the possible role of introns. J Mol Evol 2004, 58(6):712-21.
  • [36]Siaut M, Heijde M, Mangogna M, Montsant A, Coesel S, Allen A, Manfredonia A, Falciatore A, Bowler C: Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum. Gene 2007, 406:23-35.
  • [37]Nymark M, Valle KC, Hancke K, Winge P, Andresen K, Johnsen G, Bones AM, Brembu T: Molecular and Photosynthetic Responses to Prolonged Darkness and Subsequent Acclimation to Re-Illumination in the Diatom Phaeodactylum tricornutum. PLoS ONE 2013, 8:e58722.
  • [38]Oeltjen A, Krumbein WE, Rhiel E: Investigations on transcript sizes, steady-state mRNA concentrations and diurnal expression of genes encoding fucoxanthin chlorophyll a/c light-harvesting polypeptides in the centric diatom Cyclotella cryptica. Plant Biol 2002, 4:250-257.
  • [39]Maheswari U, Mock T, Armbrust EV, Bowler C: Update of the diatom EST database: a new tool for digital transcriptomics. Nucleic Acid Res 2009, 37:D1001-D1005.
  • [40]Nymark M, Valle KC, Brembu T, Hancke K, Winge P, Andresen K, Johnsen G, Bones AM: An integrated analysis of molecular acclimation to high light in the marine diatom Phaeodactylum tricornutum. PLoS One 2009, 4:e7743.
  • [41]Lepetit B, Sturm S, Rogato A, Gruber A, Sachse M, Falciatore A, Kroth PG, Lavaud J: High light acclimation in the secondary plastids containing diatom Phaeodactylum tricornutum is triggered by the redox state of the plastoquinone pool. Plant Physiol 2013, 161(2):853-865.
  • [42]Park S, Jung G, Hwang Y, Jin ES: Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to higher irradiance. Planta 2010, 231:349-360.
  • [43]Zhu SH, Green BR: Photoprotection in the diatom Thalassiosira pseudonana: Role of LI818-like proteins in response to high light stress. Biochim Biophys Acta 2010, 1797:1449-1457.
  • [44]Bailleul B, Rogata A, de Martino A, Coesel S, Cardol P, Bowler C, Falciatore A, Finazzi G: An atypical member of the light-harvesting complex stress-related protein family modulates diatom responses to light. Proc Natl Acad Sci U S A 2010, 107:18214-18219.
  • [45]Gundermann K, Schmidt M, Weisheit W, Mittag M, Büchel C: Identification of several sub-populations in the pool of light harvesting proteins in the pennate diatom Phaeodactylum tricornutum. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2013, 1827(3):303-310.
  • [46]Funk C, Alami M, Tibiletti T, Green BR: High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta. Biochim Biophys Acta 2011, 1807:841-846.
  • [47]Grouneva I, Rokka A, Aro EM: The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. J Proteome Res 2011, 10(12):5338-5353.
  • [48]Ikeda Y, Yamagishi A, Komura M, Suzuki T, Dohmae N, Shibata Y, Itoh S, Koike H, Satoh K: Two types of fucoxanthin-chlorophyll-binding proteins I tightly bound to the photosystem I core complex in marine centric diatoms. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2013, 1827(4):529-539.
  • [49]Lepetit B, Volke D, Gilbert M, Wilhelm C, Goss R: Evidence for the existence of one antenna-associated, lipid-dissolved and two protein-bound pools of diadinoxanthin cycle pigments in diatoms. Plant Physiol 2010, 154(4):1905-1920.
  • [50]Schellenberger Costa B, Jungandreas A, Jakob T, Weisheit W, Mittag M, Wilhelm C: Blue light is essential for high light acclimation and photoprotection in the diatom Phaeodactylum tricornutum. J Exp Bot 2013, 64(2):483-493.
  • [51]Lavaud J: Fast regulation of photosynthesis in diatoms: Mechanisms, evolution and ecophysiology. Plant Sci Biotechnol 2007, 1:267-287.
  • [52]Armbrust EV: The life of diatoms in the world’s oceans. Nature 2009, 459:185-192.
  • [53]Brunet C, Lavaud J: Can the xanthophyll cycle help extract the essence of the microalgal functional response to a variable light environment? J Plankton Res 2010, 32:1609-1617.
  • [54]Chauton MS, Winge P, Brembu T, Vadstein O, Bones AM: Gene regulation of carbon fixation, storage, and utilization in the diatom Phaeodactylum tricornutum acclimated to light/dark cycles. Plant Physiol 2013, 161(2):1034-1048.
  • [55]Depauw FA, Rogato A, Ribera d’Alcalá M, Falciatore A: Exploring the molecular basis of responses to light in marine diatoms. J Exp Botany 2012, 63(4):1575-1591.
  • [56]Huysman MJ, Fortunato AE, Matthijs M, Costa BS, Vanderhaeghen R, Van den Daele H, Sachse M, Inzé D, Bowler C, Kroth PG, Wilhelm C, Falciatore A, Vyverman W, De Veylder L: AUREOCHROME1a-mediated induction of the diatom-specific cyclin dsCYC2 controls the onset of cell division in diatoms (Phaeodactylum tricornutum). Plant Cell 2013, 25:215-228.
  • [57]Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, LaRoche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG: The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 2006, 157(2):91-124.
  • [58]Lepetit B, Goss R, Jakob T, Wilhelm C: Molecular dynamics of the diatom thylakoid membrane under different light conditions. Photosynth Res 2012, 111:245-57.
  • [59]Grouneva I, Gollan P, Kangasjärvi S, Suorsa M, Tikkanen M, Aro EM: Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms. Planta 2013, 237(2):399-412.
  • [60]Sarthou G, Timmermans KR, Blain S, Tréguer P: Growth physiology and fate of diatoms in the ocean: a review. J Sea Res 2005, 53:25-42.
  • [61]Phaeodactylum tricornutum v2.0 genome database http://genome.jgi-psf.org/Phatr2/Phatr2.home.html webcite
  • [62]Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, et al.: The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 2008, 456(7219):239-244.
  • [63]Thalassiosira pseudonana v3.0 genome database http://genome.jgi-psf.org/Thaps3/Thaps3.home.html webcite
  • [64]Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kröger N, Lau WWY, Lane TW, Larimer FW, Lippmeier JC, Lucas S, et al.: The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 2004, 306(5693):79-86.
  • [65]Guillardia theta CCMP2712 v1.0 genome database http://genome.jgi.doe.gov/Guith1/Guith1.home.html webcite
  • [66]Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF, Kuo A, Rensing SA, Schmutz J, Symeonidi A, Elias M, Eveleigh RJM, Herman EK, Klute MJ, Nakayama T, Oborník M, Reyes-Prieto A, Armbrust EV, Aves SJ, Beiko RG, Coutinho P, Dacks JB, Durnford DG, Fast NM, Green BR: Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 2012, 492:59-65.
  • [67]Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I: The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 2012, 40:D26-D32.
  • [68]United States Department of Energy Joint Genome Institute (JGI) http://www.jgi.doe.gov/ webcite
  • [69]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-402.
  • [70]National Center for Biotechnology Information (NCBI) http://www.ncbi.nlm.nih.gov webcite
  • [71]Cyanidioschyzon merolae Genome Project http://merolae.biol.s.u-tokyo.ac.jp/ webcite
  • [72]Michigan State University Galdieria Database http://genomics.msu.edu/galdieria webcite
  • [73]Weber A, Oesterhelt C, Gross W, Bräutigam A, Imboden L, Krassovskaya I, Linka N, Truchina J, Schneidereit J, Voll H, Voll L, Zimmermann M, Jamai A, Riekhof W, Yu B, Garavito R, Benning C: EST-analysis of the thermo-acidophilic red microalga Galdieriasulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol 2004, 55:17-32.
  • [74]Barbier G, Oesterhelt C, Larson MD, Halgren RG, Wilkerson C, Garavito RM, Benning C, Weber AP: Comparative genomics of two closely related unicellular thermo-Acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol 2005, 137:460-474.
  • [75]Universal Protein Resource (UniProt) http://www.expasy.uniprot.org/ webcite
  • [76]Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT, Wu X, Reith M, Cavalier-Smith T, Maier UG: The highly reduced genome of an enslaved algal nucleus. Nature 2001, 410:1091-1096.
  • [77]Tanifuji G, Onodera NT, Wheeler TJ, Dlutek M, Donaher N, Archibald JM: Complete Nucleomorph Genome Sequence of the Nonphotosynthetic Alga Cryptomonas paramecium Reveals a Core Nucleomorph Gene Set. Genome Biol Evol 2011, 3:44-54.
  • [78]Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM: Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci 2007, 104(50):19908-19913.
  • [79]Moore CE, Curtis B, Mills T, Tanifuji G, Archibald JM: Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol Evol 2012, 4(11):1162-1175.
  • [80]Ohta N, Matsuzaki M, Misumi O, Miyagishima Sy, Nozaki H, Tanaka K, Shin-I T, Kohara Y, Kuroiwa T: Complete sequence and analysis of the plastid genome of the unicellular red alga Cyanidioschyzon merolae. DNA Res 2003, 10(2):67-77.
  • [81]Glöckner G, Rosenthal A, Valentin K: The structure and gene repertoire of an ancient red algal plastid genome. J Mol Evol 2000, 51:382-390.
  • [82]Reith M, Munholland J: Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol Biol Report 1995, 13:333-335.
  • [83]Hagopian J, Reis M, Kitajima J, Bhattacharya D, Oliveira M: Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui provides insights into the evolution of rhodoplasts and their relationship to other plastids. J Mol Evol 2004, 59:464-477.
  • [84]Douglas SE, Penny SL: The plastid genome of the cryptophyte alga, Guillardia theta: complete sequence and conserved synteny groups confirm its common ancestry with red algae. J Mol Evol 1999, V48(2):236-244.
  • [85]Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM: Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol Evol 2007, 24(8):1832-1842.
  • [86]Donaher N, Tanifuji G, Onodera NT, Malfatti SA, Chain PSG, Hara Y, Archibald JM: The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate. Genome Biol Evol 2009, 1:439-448.
  • [87]Oudot-Le Secq MP, Grimwood J, Shapiro H, Armbrust EV, Bowler C, Green BR: Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Gen Genomics 2007, 277(4):427-439.
  • [88]Cserzö M, Wallin E, Simon I, von Heijne G, Elofsson A: Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Prot Engin 1997, 10:673-676.
  • [89]SignalP 3.0 http://www.cbs.dtu.dk/services/SignalP-3.0/ webcite
  • [90]Bendtsen JD, Nielsen H, von Heijne G, Brunak S: Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340(4):783-795.
  • [91]Notredame C, Higgins DG, Heringa J: T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000, 302:205-217.
  • [92]Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C: T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 2011, 39:W13-W17.
  • [93]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98. Nucleic Acids Symp Ser 1999, 41:95-98.
  • [94]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
  • [95]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [96]Guindon S, Lethiec F, Duroux P, Gascuel O: PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 2005, 33:W557-W559.
  • [97]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinform 2001, 17:754-755.
  • [98]Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual, 3rd ed. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1995.
  • [99]Zaslavskaia LA, Lippmeier JC, Kroth PG, Grossman AR, Apt KE: Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes. J Phycol 2000, 36(2):379-386.
  • [100]Kroth PG: Genetic transformation; a tool to study protein targeting in diatoms. Methods Mol Biol 2007, 390:257-267.
  • [101]Guillard RRL: Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrate Animals. Edited by Smith WL, Chanley MH. New York: Plenum Press; 1975:29-60.
  • [102]Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
  • [103]Sachse M, Sturm S, Gruber A, Kroth PG: Identification and evaluation of endogenous reference genes for steady state transcript quantification by qPCR in the diatom Phaeodactlyum tricornutum with constitutive expression independent from time and light. J Endocytobiosis Cell Res 2013, 24:1-7.
  • [104]Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W: Crystal structure of spinach major light-harvesting complex at 2.72Å resolution. Nature 2004, 428(6980):287-292.
  • [105]Pandit A, Morosinotto T, Reus M, Holzwarth AR, Bassi R, de Groot HJ: First solid-state {NMR} analysis of uniformly 13C-enriched major light-harvesting complexes from Chlamydomonas reinhardtii and identification of protein and cofactor spin clusters. Biochimica et Biophysica Acta (BBA) - Bioenerg 2011, 1807(4):437-443.
  • [106]Remelli R, Varotto C, Sandonà D, Croce R, Bassi R: Chlorophyll binding to monomeric light-harvesting complex - A mutation analysis of chromophore-binding residues. J Biol Chem 1999, 274(47):33510-33521.
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