Chlorella vulgaris genome assembly and annotation reveals the molecular basis for metabolic acclimation to high light conditions
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Summary: Chlorella vulgaris is a fast‐growing fresh‐water microalga cultivated on the industrial scale for applications ranging from food to biofuel production. To advance our understanding of its biology and to establish genetics tools for biotechnological manipulation, we sequenced the nuclear and organelle genomes of Chlorella vulgaris 211/11P by combining next generation sequencing and optical mapping of isolated DNA molecules. This hybrid approach allowed us to assemble the nuclear genome in 14 pseudo‐molecules with an N50 of 2.8 Mb and 98.9% of scaffolded genome. The integration of RNA‐seq data obtained at two different irradiances of growth (high light, HL versus low light, LL) enabled us to identify 10 724 nuclear genes, coding for 11 082 transcripts. Moreover, 121 and 48 genes, respectively, were found in the chloroplast and mitochondrial genome. Functional annotation and expression analysis of nuclear, chloroplast and mitochondrial genome sequences revealed particular features of Chlorella vulgaris . Evidence of horizontal gene transfers from chloroplast to mitochondrial genome was observed. Furthermore, comparative transcriptomic analyses of LL versus HL provided insights into the molecular basis for metabolic rearrangement under HL versus LL conditions leading to enhanced de novo fatty acid biosynthesis and triacylglycerol accumulation. The occurrence of a cytosolic fatty acid biosynthetic pathway could be predicted and its upregulation upon HL exposure was observed, consistent with the increased lipid amount under HL conditions. These data provide a rich genetic resource for future genome editing studies, and potential targets for biotechnological manipulation of Chlorella vulgaris or other microalgae species to improve biomass and lipid productivity.
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Analysis of gene expression involved in lipid production at the transcriptome level in microalgae has offered valuable insights into metabolic pathways and contextual information regarding genomic-level modifications in algae.
“In recent years, analysis of gene expression involved in lipid production at the transcriptome level in microalgae has offered valuable insights into metabolic pathways, as well as contextual information regarding modifications at the genomic level in algae [231–234].”
From Microalgae biofuels: illuminating the path to a sustainable future amidst challenges and opportunities (2024) · cites this paper as [232]
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A RAPID METHOD OF TOTAL LIPID EXTRACTION AND PURIFICATION
Bligh, E. G., & Dyer, W. J. (1959) · Canadian Journal of Biochemistry and Physiology · doi:10.1139/o59-099 · Cited by 54,751 · see citing works
Vieler, A., Wu, G., Tsai, C.-H., Bullard, B., Cornish, A. J., Harvey, C., Reca, I.-B., Thornburg, C., Achawanantakun, R., Buehl, C. J., et al. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1003064 · Cited by 458 · see citing works
Gao, C., Wang, Y., Shen, Y., Yan, D., He, X., Dai, J., & Wu, Q. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-582 · Cited by 175 · see citing works
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Research works printed but not linked: 94
- Ajjawi, I., Verruto, J., Aqui, M. et al. (2017) Lipid production in Nannochloropsis gaditana is doubled by decreasing expression of a single transcriptional regulator. Nat. Biotechnol. 35, 647. 28628130
- Alboresi, A., Perin, G., Vitulo, N. et al. (2016) Light remodels lipid biosynthesis in Nannochloropsis gaditana by modulating carbon partitioning between organelles. Plant Physiol. 171, 2468– 2482. 27325666 PMC4972283
- Allen, M.M. and Stanier, R.Y. (1968) Growth and division of some unicellular blue‐green algae. J. Gen. Microbiol. 51, 199– 202. 5652095
- Allorent, G., Lefebvre‐Legendre, L., Chappuis, R., Kuntz, M., Truong, T.B., Niyogi, K.K., Ulm, R. and Goldschmidt‐Clermont, M. (2016) UV‐B photoreceptor‐mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA, 113, 14864– 14869. 27930292 PMC5187749
- Arriola, M., Velmurugan, N., Zhang, Y., Plunkett, M., Hondzo, H. and Barney, B. (2018) Genome sequences of Chlorella sorokiniana UTEX 1602 and Micractinium conductrix SAG 241.80: implications to maltose excretion by a green alga. Plant J. 93, 566– 586. 29178410
- Ballottari, M., Dall'Osto, L., Morosinotto, T. and Bassi, R. (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947– 8958. 17229724
- Berteotti, S., Ballottari, M. and Bassi, R. (2016) Increased biomass productivity in green algae by tuning non‐photochemical quenching. Sci. Rep. 6, 21339. 26888481 PMC4758054
- Blaby, I.K., Blaby‐Haas, C.E., Tourasse, N. et al. (2014) The Chlamydomonas genome project: a decade on. Trends Plant Sci. 19, 672– 680. 24950814 PMC4185214
- Blanc, G., Duncan, G., Agarkova, I. et al. (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell, 22, 2943– 2955. 20852019 PMC2965543
- Blanc, G., Agarkova, I., Grimwood, J. et al. (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol. 13, R39. 22630137 PMC3446292
- Bonente, G., Pippa, S., Castellano, S., Bassi, R. and Ballottari, M. (2012) Acclimation of Chlamydomonas reinhardtii to different growth irradiances. J. Biol. Chem. 287, 5833– 5847. 22205699 PMC3285353
- Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M. and Rochaix, J.D. (1997) The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16, 6095– 6104. 9321389 PMC1326293
- Boyle, N. and Morgan, J. (2009) Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst. Biol. 3, 4. 19128495 PMC2628641
- Cecchin, M., Benfatto, S., Griggio, F., Mori, A., Cazzaniga, S., Vitulo, N., Delledonne, M. and Ballottari, M. (2018) Molecular basis of autotrophic versus mixotrophic growth in Chlorella sorokiniana. Sci. Rep. 8, 6465. 29691462 PMC5915390
- Charuchinda, P., Waditee‐Sirisattha, R., Kageyama, H., Yamada, D., Sirisattha, S., Tanaka, Y., Mahakhant, A. and Takabe, T. (2015) Caleosin from Chlorella vulgaris TISTR 8580 is salt‐induced and heme‐containing protein. Biosci. Biotechnol. Biochem. 79, 1119– 1124. 25703935
- Chin, C.S., Peluso, P., Sedlazeck, F.J. et al. (2016) Phased diploid genome assembly with single‐molecule real‐time sequencing. Nat. Methods, 13, 1050– 1054. 27749838 PMC5503144
- Conesa, A., Gotz, S., Garcia‐Gomez, J., Terol, J., Talon, M. and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674– 3676. 16081474
- Correa‐Galvis, V., Redekop, P., Guan, K., Griess, A., Truong, T.B., Wakao, S., Niyogi, K.K. and Jahns, P. (2016) Photosystem II subunit PsbS Is involved in the induction of LHCSR protein‐dependent energy dissipation in Chlamydomonas reinhardtii. J. Biol. Chem. 291, 17478– 17487. 27358399 PMC5016143
- Corteggiani Carpinelli, E., Telatin, A., Vitulo, N., Forcato, C., D'Angelo, M., Schiavon, R., Vezzi, A., Giacometti, G.M., Morosinotto, T. and Valle, G. (2014) Chromosome scale genome assembly and transcriptome profiling of Nannochloropsis gaditana in nitrogen depletion. Mol. Plant, 7, 323– 335. 23966634
- Dall'Osto, L., Cazzaniga, S., North, H., Marion‐Poll, A. and Bassi, R. (2007) The Arabidopsis aba4‐1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell, 19, 1048– 1064. 17351115 PMC1867355
- Daniell, H., Lin, C.S., Yu, M. and Chang, W.J. (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol. 17, 134. 27339192 PMC4918201
- Denovan‐Wright, E.M., Nedelcu, A.M. and Lee, R.W. (1998) Complete sequence of the mitochondrial DNA of Chlamydomonas eugametos. Plant Mol. Biol. 36, 285– 295. 9484440
- Dereeper, A., Guignon, V., Blanc, G. et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non‐specialist. Nucleic Acids Res. 36, W465– W469. 18424797 PMC2447785
- Desplats, C., Mus, F., Cuiné, S., Billon, E., Cournac, L. and Peltier, G. (2009) Characterization of Nda2, a plastoquinone‐reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284, 4148– 4157. 19056727
- Driver, T., Trivedi, D.K., McIntosh, O.A., Dean, A.P., Goodacre, R. and Pittman, J.K. (2017) Two Glycerol‐3‐Phosphate Dehydrogenases from Chlamydomonas have distinct roles in lipid metabolism. Plant Physiol. 174, 2083– 2097. 28588114 PMC5543956
- Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113. 15318951 PMC517706
- Gandini, C.L. and Sanchez‐Puerta, M.V. (2017) Foreign plastid sequences in plant mitochondria are frequently acquired via mitochondrion‐to‐mitochondrion horizontal transfer. Sci. Rep. 7, 43402. 28262720 PMC5338292
- Goremykin, V.V., Salamini, F., Velasco, R. and Viola, R. (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol. Biol. Evol. 26, 99– 110. 18922764
- Guarnieri, M.T., Levering, J., Henard, C.A., Boore, J.L., Betenbaugh, M.J., Zengler, K. and Knoshaug, E.P. (2018) Genome sequence of the Oleaginous Green Alga, Chlorella vulgaris UTEX 395. Front. Bioeng. Biotechnol. 6, 37. 29675409 PMC5895722
- Heimerl, N., Hommel, E., Westermann, M., Meichsner, D., Lohr, M., Hertweck, C., Grossman, A.R., Mittag, M. and Sasso, S. (2018) A giant type I polyketide synthase participates in zygospore maturation in Chlamydomonas reinhardtii. Plant J. 95, 268– 281. 29729034
- Houille‐Vernes, L., Rappaport, F., Wollman, F.A., Alric, J. and Johnson, X. (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl. Acad. Sci. USA, 108, 20820– 20825. 22143777 PMC3251066
- Huang, N.L., Huang, M.D., Chen, T.L. and Huang, A.H. (2013) Oleosin of subcellular lipid droplets evolved in green algae. Plant Physiol. 161, 1862– 1874. 23391579 PMC3613461
- Johnson, X., Steinbeck, J., Dent, R.M. et al. (2014) Proton gradient regulation 5‐mediated cyclic electron flow under ATP‐ or redox‐limited conditions: a study of ΔATpase pgr5 and ΔrbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol. 165, 438– 452. 24623849 PMC4012601
- Juneja, A., Chaplen, F. and Murthy, G. (2016) Genome scale metabolic reconstruction of Chlorella variabilis for exploring its metabolic potential for biofuels. Biores. Technol. 213, 103– 110. 26995318
- Kanehisa, M. and Goto, S. (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27– 30. 10592173 PMC102409
- Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M. and Tanabe, M. (2016) KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 44, D457– D462. 26476454 PMC4702792
- Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y. and Morishima, K. (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45, D353– D361. 27899662 PMC5210567
- Kim, D., Langmead, B. and Salzberg, S.L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nat. Methods, 12, 357– 360. 25751142 PMC4655817
- Kirst, H., Gabilly, S.T., Niyogi, K.K., Lemaux, P.G. and Melis, A. (2017) Photosynthetic antenna engineering to improve crop yields. Planta, 245, 1009– 1020. 28188423
- Kobayashi, K. (2016) Role of membrane glycerolipids in photosynthesis, thylakoid biogenesis and chloroplast development. J. Plant. Res. 129, 565– 580. 27114097 PMC5897459
- Kong, F., Liang, Y., Légeret, B., Beyly‐Adriano, A., Blangy, S., Haslam, R.P., Napier, J.A., Beisson, F., Peltier, G. and Li‐Beisson, Y. (2017) Chlamydomonas carries out fatty acid β‐oxidation in ancestral peroxisomes using a bona fide acyl‐CoA oxidase. Plant J. 90, 358– 371. 28142200
- Kouřil, R., Nosek, L., Bartoš, J., Boekema, E.J. and Ilík, P. (2016) Evolutionary loss of light‐harvesting proteins Lhcb6 and Lhcb3 in major land plant groups–break‐up of current dogma. New Phytol. 210, 808– 814. 27001142
- Kromdijk, J., Głowacka, K., Leonelli, L., Gabilly, S.T., Iwai, M., Niyogi, K.K. and Long, S.P. (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354, 857– 861. 27856901
- Li, X.P., Björkman, O., Shih, C., Grossman, A.R., Rosenquist, M., Jansson, S. and Niyogi, K.K. (2000) A pigment‐binding protein essential for regulation of photosynthetic light harvesting. Nature, 403, 391– 395. 10667783
- Lin, M. and Oliver, D.J. (2008) The role of acetyl‐coenzyme a synthetase in Arabidopsis. Plant Physiol. 147, 1822– 1829. 18552233 PMC2492652
- Lin, I.P., Jiang, P.L., Chen, C.S. and Tzen, J.T. (2012) A unique caleosin serving as the major integral protein in oil bodies isolated from Chlorella sp. cells cultured with limited nitrogen. Plant Physiol. Biochem. 61, 80– 87. 23085585
- Lohse, M., Drechsel, O., Kahlau, S. and Bock, R. (2013) OrganellarGenomeDRAW–a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 41, W575– W581. 23609545 PMC3692101
- Love, M.I., Huber, W. and Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA‐seq data with DESeq2. Genome Biol. 15, 550. 25516281 PMC4302049
- Lum, K.K., Kim, J. and Lei, X.G. (2013) Dual potential of microalgae as a sustainable biofuel feedstock and animal feed. J. Anim. Sci. Biotechnol. 4, 53. 24359607 PMC3881014
- Lv, J.M., Cheng, L.H., Xu, X.H., Zhang, L. and Chen, H.L. (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour. Technol. 101, 6797– 6804. 20456951
- Malik, S.B., Pightling, A.W., Stefaniak, L.M., Schurko, A.M. and Logsdon, J.M. (2007) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE, 3, e2879. 18663385 PMC2488364
- Maul, J.E., Lilly, J.W., Cui, L., dePamphilis, C.W., Miller, W., Harris, E.H. and Stern, D.B. (2002) The Chlamydomonas reinhardtii plastid chromosome: islands of genes in a sea of repeats. Plant Cell, 14, 2659– 2679. 12417694 PMC153795
- Merchant, S.S., Prochnik, S.E., Vallon, O. et al. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318, 245– 250. 17932292 PMC2875087
- Moellering, E.R. and Benning, C. (2010) RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryot. Cell, 9, 97– 106. 19915074 PMC2805299
- Moore, E.R., Bullington, B.S., Weisberg, A.J., Jiang, Y., Chang, J. and Halsey, K.H. (2017) Morphological and transcriptomic evidence for ammonium induction of sexual reproduction in Thalassiosira pseudonana and other centric diatoms. PLoS ONE, 12, e0181098. 28686696 PMC5501676
- Murphy, D.J. (2012) The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma, 249, 541– 585. 22002710
- Naduthodi, M.I.S., Barbosa, M.J. and van der Oost, J. (2018) Progress of CRISPR‐Cas based genome editing in photosynthetic microbes. Biotechnol. J. 13, e1700591. 29396999
- Nguyen, H.M., Cuiné, S., Beyly‐Adriano, A., Légeret, B., Billon, E., Auroy, P., Beisson, F., Peltier, G. and Li‐Beisson, Y. (2013) The green microalga Chlamydomonas reinhardtii has a single ω‐3 fatty acid desaturase that localizes to the chloroplast and impacts both plastidic and extraplastidic membrane lipids. Plant Physiol. 163, 914– 928. 23958863 PMC3793068
- Ort, D.R., Merchant, S.S., Alric, J. et al. (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. USA, 112, 8529– 8536. 26124102 PMC4507207
- Peers, G., Truong, T.B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A.R., Hippler, M. and Niyogi, K.K. (2009) An ancient light‐harvesting protein is critical for the regulation of algal photosynthesis. Nature, 462, 518– 521. 19940928
- Petroutsos, D., Terauchi, A.M., Busch, A., Hirschmann, I., Merchant, S.S., Finazzi, G. and Hippler, M. (2009) PGRL1 participates in iron‐induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J. Biol. Chem. 284, 32770– 32781. 19783661 PMC2781694
- Plancke, C., Vigeolas, H., Höhner, R. et al. (2014) Lack of isocitrate lyase in Chlamydomonas leads to changes in carbon metabolism and in the response to oxidative stress under mixotrophic growth. Plant J. 77, 404– 417. 24286363
- Poliner, E., Panchy, N., Newton, L., Wu, G., Lapinsky, A., Bullard, B., Zienkiewicz, A., Benning, C., Shiu, S.H. and Farré, E.M. (2015) Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCMP1779 under light/dark cycles. Plant J. 83, 1097– 1113. 26216534
- Radakovits, R., Jinkerson, R.E., Fuerstenberg, S.I., Tae, H., Settlage, R.E., Boore, J.L. and Posewitz, M.C. (2012) Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat. Commun. 3, 686. 22353717 PMC3293424
- Roth, M.S., Cokus, S.J., Gallaher, S.D. et al. (2017) Chromosome‐level genome assembly and transcriptome of the green alga Chromochloris zofingiensis illuminates astaxanthin production. Proc. Natl. Acad. Sci. USA, 114, E4296– E4305. 28484037 PMC5448231
- Rufty, T.W. and Huber, S.C. (1983) Changes in starch formation and activities of sucrose phosphate synthase and cytoplasmic fructose‐1,6‐bisphosphatase in response to source‐sink alterations. Plant Physiol. 72, 474– 480. 16663027 PMC1066258
- Rumeau, D., Peltier, G. and Cournac, L. (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30, 1041– 1051. 17661746
- Saroussi, S.I., Wittkopp, T.M. and Grossman, A.R. (2016) The type II NADPH dehydrogenase facilitates cyclic electron flow, energy‐dependent quenching, and chlororespiratory metabolism during acclimation of Chlamydomonas reinhardtii to nitrogen deprivation. Plant Physiol. 170, 1975– 1988. 26858365 PMC4825143
- Scheller, H.V., Jensen, P.E., Haldrup, A., Lunde, C. and Knoetzel, J. (2001) Role of subunits in eukaryotic Photosystem I. Biochim. Biophys. Acta, 1507, 41– 60. 11687207
- Schweizer, E. and Hofmann, J. (2004) Microbial type I fatty acid synthases (FAS): major players in a network of cellular FAS systems. Microbiol. Mol. Biol. Rev. 68, 501– 517. table of contents. 15353567 PMC515254
- Shi, L.X. and Schröder, W.P. (2004) The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta, 1608, 75– 96. 14871485
- Shi, L.X., Kim, S.J., Marchant, A., Robinson, C. and Schröder, W.P. (1999) Characterisation of the PsbX protein from Photosystem II and light regulation of its gene expression in higher plants. Plant Mol. Biol. 40, 737– 744. 10480397
- Shi, L.X., Hall, M., Funk, C. and Schröder, W.P. (2012) Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins. Biochim. Biophys. Acta, 1817, 13– 25. 21907181
- Shimada, H., Fukuta, M., Ishikawa, M. and Sugiura, M. (1990) Rice chloroplast RNA polymerase genes: the absence of an intron in rpoC1 and the presence of an extra sequence in rpoC2. Mol. Gen. Genet. 221, 395– 402. 2381420
- Siaut, M., Cuiné, S., Cagnon, C. et al. (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol. 11, 7. 21255402 PMC3036615
- Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V. and Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single‐copy orthologs. Bioinformatics, 31, 3210– 3212. 26059717
- Smith, S. and Tsai, S.C. (2007) The type I fatty acid and polyketide synthases: a tale of two megasynthases. Nat. Prod. Rep. 24, 1041– 1072. 17898897 PMC2263081
- Soorni, A., Haak, D., Zaitlin, D. and Bombarely, A. (2017) Organelle_PBA, a pipeline for assembling chloroplast and mitochondrial genomes from PacBio DNA sequencing data. BMC Genom. 18, 49. PMC5219736 28061749
- Specht, M., Stanke, M., Terashima, M., Naumann‐Busch, B., Janssen, I., Höhner, R., Hom, E.F., Liang, C. and Hippler, M. (2011) Concerted action of the new Genomic Peptide Finder and AUGUSTUS allows for automated proteogenomic annotation of the Chlamydomonas reinhardtii genome. Proteomics, 11, 1814– 1823. 21432999 PMC3145493
- Staňková, H., Hastie, A.R., Chan, S. et al. (2016) BioNano genome mapping of individual chromosomes supports physical mapping and sequence assembly in complex plant genomes. Plant Biotechnol. J. 14, 1523– 1531. 26801360 PMC5066648
- Straub, S., Cronn, R., Edwards, C., Fishbein, M. and Liston, A. (2013) Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (Apocynaceae). Genome Biol. Evol. 5, 1872– 1885. 24029811 PMC3814198
- Tardif, M., Atteia, A., Specht, M. et al. (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol. Biol. Evol. 29, 3625– 3639. 22826458
- Tibiletti, T., Auroy, P., Peltier, G. and Caffarri, S. (2016) Chlamydomonas reinhardtii PsbS protein is functional and accumulates rapidly and transiently under high light. Plant Physiol. 171, 2717– 2730. 27329221 PMC4972282
- Tillich, M., Lehwark, P., Pellizzer, T., Ulbricht‐Jones, E.S., Fischer, A., Bock, R. and Greiner, S. (2017) GeSeq ‐ versatile and accurate annotation of organelle genomes. Nucleic Acids Res. 45, W6– W11. 28486635 PMC5570176
- Wakasugi, T., Nagai, T., Kapoor, M. et al. (1997) Complete nucleotide sequence of the chloroplast genome from the green alga Chlorella vulgaris: the existence of genes possibly involved in chloroplast division. Proc. Natl Acad. Sci. USA, 94, 5967– 5972. 9159184 PMC20890
- Wang, D., Wu, Y.W., Shih, A.C., Wu, C.S., Wang, Y.N. and Chaw, S.M. (2007) Transfer of chloroplast genomic DNA to mitochondrial genome occurred at least 300 MYA. Mol. Biol. Evol. 24, 2040– 2048. 17609537
- Waterhouse, R.M., Seppey, M., Simão, F.A., Manni, M., Ioannidis, P., Klioutchnikov, G., Kriventseva, E.V. and Zdobnov, E.M. (2017) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 35, 543– 548. PMC5850278 29220515
- Wong, J.L. and Johnson, M.A. (2010) Is HAP2‐GCS1 an ancestral gamete fusogen? Trends Cell Biol. 20, 134– 141. 20080406
- Yamamoto, M., Fujishita, M., Hirata, A. and Kawano, S. (2004) Regeneration and maturation of daughter cell walls in the autospore‐forming green alga Chlorella vulgaris (Chlorophyta, Trebouxiophyceae). J. Plant. Res. 117, 257– 264. 15108033
- Yoshinaga, Y., Daum, C., He, G. and O'Malley, R. (2018) Genome sequencing. Methods Mol. Biol. 1775, 37– 52. 29876807
- Youssef, A., Laizet, Y., Block, M.A., Maréchal, E., Alcaraz, J.P., Larson, T.R., Pontier, D., Gaffé, J. and Kuntz, M. (2010) Plant lipid‐associated fibrillin proteins condition jasmonate production under photosynthetic stress. Plant J. 61, 436– 445. 19906042
- Zäuner, S., Jochum, W., Bigorowski, T. and Benning, C. (2012) A cytochrome b5‐containing plastid‐located fatty acid desaturase from Chlamydomonas reinhardtii. Eukaryot. Cell, 11, 856– 863. 22562471 PMC3416504
- Zhong, Y.J., Huang, J.C., Liu, J., Li, Y., Jiang, Y., Xu, Z.F., Sandmann, G. and Chen, F. (2011) Functional characterization of various algal carotenoid ketolases reveals that ketolating zeaxanthin efficiently is essential for high production of astaxanthin in transgenic Arabidopsis. J. Exp. Bot. 62, 3659– 3669. 21398427 PMC3130182
- Zuniga, C., Li, C., Huelsman, T. et al. (2016) Genome‐scale metabolic model for the green alga Chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions. Plant Physiol. 172, 589– 602. 27372244 PMC5074608
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Wang, M., Ye, X., Bi, H., & Shen, Z. (2024) · Biotechnology for Biofuels and Bioproducts · doi:10.1186/s13068-024-02461-0 · Cited by 201 · see citing works
Ng, I., Keskin, B. B., & Tan, S. (2020) · Biotechnology Journal · doi:10.1002/biot.201900228 · Cited by 135 · see citing works
- Authors
- Cecchin, M., Marcolungo, L., Rossato, M., Girolomoni, L., Cosentino, E., Cuine, S., Li‐Beisson, Y., Delledonne, M., & Ballottari, M.
- Affiliations
- University of Verona (IT)
- Institute of Biosciences and Biotechnologies of Aix‐Marseille, UMR7265 Aix‐Marseille University CEA CNRS CEA Cadarache Saint‐Paul‐lez Durance F‐13108 France
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Ballottari, Matteo
- ORCID
- Venue
- The Plant Journal
- Publisher
- Wiley
- Published
- 2019-09-24
- Volume
- 100
- Issue
- 6
- Pages
- 1289-1305
- ISSN
- 0960-7412 (ISSN-L)
- 1365-313X
- PMC
- PMC6972661
- OpenAlex
- W2969593367
- Cited by
- 83
- References
- 3
- Citations by year
- 2026: 14 · 2025: 15 · 2024: 23 · 2023: 6 · 2022: 10 · 2021: 11 · 2020: 4
- FWCI
- 1.33
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Plant Journal (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL AMU (submittedVersion)
- Funders
- H2020 European Research Council (679814)
- Topics
- Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Keywords
- Chlorella vulgaris, genome assembly, genome annotation, high light acclimation, chloroplast genome, mitochondrial genome, horizontal gene transfer, fatty acid synthesis, triglyceride accumulation, lipid metabolism, transcriptome, microalgae, biofuel feedstock
- MeSH terms
- Acclimatization, Base Sequence, Biotechnology, Fatty Acids, Light, Lipids, Meiosis, Phylogeny, Triglycerides, Gene Expression Regulation, Plant, Biomass, Genome, Plant, Gene Transfer, Horizontal, Chlorella vulgaris, Biosynthetic Pathways, Genome, Mitochondrial, Biofuels, Molecular Sequence Annotation, Transcriptome, Gene Ontology, Fatty Acid Synthases
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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