Downregulation of a putative plastid PDC E1α subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii

Journal of Experimental Botany

Volumn 65, Issue 22, 2014, Pages 6563-6576

  Shtaida, Nastassia ^a   Khozin Goldberg, Inna ^a   Solovchenko, Alexei ^b   Chekanov, Konstantin ^b   Didi Cohen, Shoshana ^a   Leu, Stefan ^a   Cohen, Zvi ^a   Boussiba, Sammy ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Acetyl CoA; chlorophyll fluorescence transients; fatty acid synthesis; lipid; microalgae; photosystem II; pyruvate dehydrogenase

Indexed keywords

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

CAROTENOID; FATTY ACID; NITROGEN; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE E1ALPHA SUBUNIT; TRIACYLGLYCEROL;

AUTOTROPHY; BIOLOGY; BIOMASS; CHLAMYDOMONAS REINHARDTII; DEFICIENCY; DOWN REGULATION; ENZYMOLOGY; GENE SILENCING; GENETIC TRANSFORMATION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT GENE; PLASTID; RADIATION RESPONSE;

AUTOTROPHIC PROCESSES; BIOMASS; CAROTENOIDS; CHLAMYDOMONAS REINHARDTII; COMPUTATIONAL BIOLOGY; DOWN-REGULATION; FATTY ACIDS; GENE SILENCING; GENES, PLANT; LIGHT; NITROGEN; PHOTOSYNTHESIS; PLASTIDS; PYRUVATE DEHYDROGENASE (LIPOAMIDE); TRANSFORMATION, GENETIC; TRIGLYCERIDES;

EID: 84922442270     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru374     Document Type: Article

References (50)

1. Behal RH, Lin M, Back S, Oliver DJ. 2002. Role of acetyl-coenzyme A synthetase in leaves of Arabidopsis thaliana. Archives of Biochemistry and Biophysics 402, 259-267
2. Blaby IK, Glaesener AG, Mettler T, et al. 2013. Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25, 4305-4523
3. Bligh EG, Dyer WJ. 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911-917
4. Bohne AV, Schwarz C, Schottkowsk M, Lidschreiber M, Piotrowski M, Zerges W, Nickelsen J. 2013. Reciprocal regulation of protein synthesis and carbon metabolism for thylakoid membrane biogenesis. PLoS Biology 11, 1-18
5. Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB, Arondel V. 2011. Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proceedings of the National Academy of Sciences, USA 108, 12527-12532
6. Boyle NR, Page MD, Liu B, et al. 2012. Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. Journal of Biological Chemistry 287, 15811-15825
7. Bustin SA, Benes V, Garson JA, et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611-622
8. Cerutti H, Ma X, Msanne J, Repas T. 2011. RNA-Mediated silencing in algae: biological roles and tools for analysis of gene function. Eukaryotic Cell 10, 1164-1172
9. Chapman KD, Dyer JM, Mullen RT. 2013. Commentary: Why dont plant leaves get fat? Plant Science 207, 128-134
10. Davey MP, Horst I, Duong GH, Tomsett E, Litvinenko AC, Howe CJ, Smith AG. 2014. Triacylglyceride production and autophagous responses in Chlamydomonas reinhardtii depend on resource allocation and carbon source. Eukaryotic Cell 3, 392-400
11. Emanuelsson O, Nielsen H, Brunak S, Von Heijne GJ. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. Journal of Molecular Biology 300, 1005-1016
12. Facchinelli F, Weber APM. 2011. The metabolite transporters of the plastid envelope: an update. Frontiers in Plant Science 2, 50
13. Fan J, Andre C, Xu C. 2011. A chloroplast pathway for the de novo biosynthesis of triacylglycerol in Chlamydomonas reinhardtii. FEBS Letters 585, 1985-1991
14. Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C. 2012. Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant and Cell Physiology 53:1380-1390
15. Giroud C, Gerber A, Eichenberger W. 1988. Lipids of Chlamydomonas reinhardtii. Analysis of molecular species and intracellular site(s) of biosynthesis. Plant and Cell Physiology 29, 587-595
16. Goodenough U, Blaby I, Casero D, et al. 2014. The path to triacylglyceride obesity in the sta6 strain of Chlamydomonas reinhardtii. Eukaryotic Cell 13, 591-613
17. Goodson C, Roth R, Wang ZT, Goodenough U. 2011. Structural correlates of cytoplasmic and chloroplast lipid body synthesis in Chlamydomonas reinhardtii and stimulation of lipid body production with acetate boost. Eukaryotic Cell 10, 1592-1606
18. Harris E. 1989. The Chlamydomonas sourcebook . San Diego, CA: Academic Press
19. Heddad, M, Willig A, Delessert C, Rahire M, Rochaix JD. 2006. DNA analysis. In: EMBO Practical Course. Molecular Genetics of Chlamydomonas. Laboratory protocols . http://www.chlamy.org/methods. html
20. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A. 2008. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and adVances. Plant Journal 54, 621-639
21. Jinkerson RE, Radakovits R, Posewitz MC. 2013. Genomic insights from the oleaginous model alga Nannochloropsis gaditana. Bioengineered 4, 37-43
22. Ke J, Behal RH, Back SL, Nikolau BJ, Wurtele ES, Oliver DJ. 2000. The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant Physiology 123, 497-508
23. Khozin-Goldberg I, Shrestha P, Cohen Z. 2005. Mobilization of arachidonyl moieties from triacylglycerols into chloroplastic lipids following recovery from nitrogen starvation of the microalga Parietochloris incisa. Biochimica et Biophysica Acta 1738, 63-71
24. Kindle KL. 1990. High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences, USA 87, 1228-1232
25. Klein U. 1986. Compartmentation of glycolysis and of the oxidative pentose-phosphate pathway in Chlamydomonas reinhardii. Planta 167, 81-86
26. Li J, Han D, Wang D, Ning K, et al. 2014. Choreography of transcriptomes and lipidomes of Nannochloropsis reveals the mechanisms of oil synthesis in microalgae Plant Cell 26, 1645-1665
27. Li X, Moellering ER, Liu B, Johnny C, Fedewa M, Sears BB, Kuo MH, Benning C. 2012. A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24, 4670-4686
28. Lin M, Behal R, Oliver DJ. 2003. Disruption of plE2, the gene for the E2 subunit of the plastid pyruvate dehydrogenase complex, in Arabidopsis causes an early embryo lethal phenotype. Plant Molecular Biology 52, 865-872
29. Lin M, Oliver DJ. 2008. The role of acetyl-coenzyme A synthetase in Arabidopsis. Plant Physiology 147, 1822-1829
30. Liu B, Benning C. 2013. Lipid metabolism in microalgae distinguishes itself. Current Opinion in Biotechnology 24, 300-309
31. Lohr M, Im CS, Grossman AR. 2005. Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiology 138, 490-515
32. Maxwell K, Johnson G. 2000. Chlorophyll fluorescence-A practical guide. Journal of Experimental Botany 51, 659-668
33. Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J. 2012. TAG, youre it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Current Opinion in Biotechnology 23, 352-363
34. Moellering ER, Benning C. 2010. RNA interference silencing of a major lipid droplet protein affects lipid droplet size in Chlamydomonas reinhardtii. Eukaryotic Cell 9, 97-106
35. Molnar A, Bassett A, Thuenemann E, Schwach F, Karkare S, Ossowski S, Weigel D, Baulcombe D. 2009. Highly specific gene silencing by artificial microRNAs in the unicellular alga Chlamydomonas reinhardtii. The Plant Journal 58, 165-174
36. Pal D, Khozin-Goldberg I, Didi-Cohen S, Solovchenko A, Batushansky A, Kaye Y, Sikron N, Samani T, Fait A, Boussiba S. 2013. Growth, lipid production and metabolic adjustments in the euryhaline eustigmatophyte Nannochloropsis oceanica CCALA 804 in response to osmotic downshift. Applied Microbiology and Biotechnology 97, 8291-8306
37. Perez-Perez ME, Florencio FJ, Crespo JL. 2010. Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiology 152, 1874-1888
38. Reid EE, Thompson P, Lyttle CR, Dennis DT. 1977. Pyruvate dehydrogenase complex from higher plant mitochondria and proplastids. Plant Physiology 59, 842-848
39. Rismani-Yazdi H, Haznedaroglu BZ, Hsin C, Peccia J. 2012. Transcriptomic analysis of the oleaginous microalga Neochloris oleoabundans reveals metabolic insights into triacylglyceride accumulation. Biotechnology for Biofuels 5, 74
40. Sakurai K, Moriyama T, Sato N. 2014. Detailed identification of fatty acid isomers sheds light on the probable precursors of triacylglycerol accumulation in photoautotrophically grown Chlamydomonas reinhardtii. Eukaryotic Cell 13, 256-266
41. Siaut M, Cuin S, Cagnon C, Fessler B, et al. 2011. Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnology 11, 7
42. Smith SR, Abbriano RM, Hildebrand M. 2012. Comparative analysis of diatom genomes reveals substantial differences in the organization of carbon partitioning pathways. Algal Research 1, 2-16
43. Solovchenko A. 2012. Physiological role of neutral lipid accumulation in eukaryotic microalgae under stresses. Russian Journal of Plant Physiology 59, 167-176
44. Solovchenko A, Solovchenko O, Khozin-Goldberg I, Didi-Cohen S, Pal D, Cohen Z, Boussiba S. 2013. Probing the effects of highlight stress on pigment and lipid metabolism in nitrogen-starving microalgae by measuring chlorophyll fluorescence transients: studies with a 5 desaturase mutant of Parietochloris incisa (Chlorophyta, Trebouxiophyceae). Algal Research 2, 175-182
45. Strasser R, Tsimilli-Michael M, Srivastava A. 2004. Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G, Govindjee, eds. Chlorophyll a fluorescence: a signature of photosynthesis . Heidelberg: Springer, 321-362
46. Tardif M, Atteia A, Specht M, et al. 2012. PredAlgo: A new subcellular localization prediction tool dedicated to green algae. Molecular Biology and Evolution 29, 3625-3639
47. Terashima M, Specht M, Hippler M. 2011. The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Current Genetics 57, 151-168
48. Wase N, Black PN, Stanley BA, DiRusso CC. 2014. Integrated quantitative analysis of nitrogen stress response in Chlamydomonas reinhardtii using metabolite and protein profiling. Journal of Proteome Research 13, 1373-1396
49. Williams JA, Dijk K, Sarka N. 2011. Selectable and inheritable gene silencing through RNA interference in the unicellular alga Chlamydomonas reinhardtii. In: Williams JA, ed. Strain engineering . New York: Humana Press, 457-476
50. Work VH, Radakovits R, Jinkerson RE, Meuser JE, Elliott LG, Vinyard DJ, Laurens LM, Dismukes GC, Posewitz MC. 2010. Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. Eukaryotic Cell 9, 1251-1261