Algal dual-specificity tyrosine phosphorylation-regulated kinase, triacylglycerol accumulation regulator1, regulates accumulation of triacylglycerol in nitrogen or sulfur deficiency

Plant Physiology

Volumn 168, Issue 2, 2015, Pages 752-764

  Kajikawa, Masataka ^a   Sawaragi, Yuri ^a   Shinkawa, Haruka ^a   Yamano, Takashi ^a   Ando, Akira ^b   Kato, Misako ^b   Hirono, Masafumi ^c,d   Sato, Naoki ^c   Fukuzawa, Hideya ^a  

^a KYOTO UNIVERSITY   (Japan)

^b OCHANOMIZU UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d HOSEI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; SACCHAROMYCES CEREVISIAE;

FAT DROPLET; NITROGEN; PLANT PROTEIN; STARCH; SULFUR; TRIACYLGLYCEROL; TYROSINE;

BIOLOGICAL MODEL; CHEMISTRY; CHLAMYDOMONAS REINHARDTII; DEFICIENCY; DRUG EFFECTS; ENZYMOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; PHOSPHORYLATION; PHYLOGENY; PLANT GENE; PROTEIN TERTIARY STRUCTURE;

CHLAMYDOMONAS REINHARDTII; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LIPID DROPLETS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; NITROGEN; PHENOTYPE; PHOSPHORYLATION; PHYLOGENY; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; STARCH; SULFUR; TRIGLYCERIDES; TYROSINE;

EID: 84933039892     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00319     Document Type: Article

References (54)

1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106
2. Aranda S, Laguna A, de la Luna S (2011) DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J 25: 449–462
3. Becker W (2012) Emerging role of DYRK family protein kinases as regulators of protein stability in cell cycle control. Cell Cycle 11: 3389–3394
4. Bellou S, Aggelis G (2012) Biochemical activities in Chlorella sp. and Nannochloropsis salina during lipid and sugar synthesis in a lab-scale open pond simulating reactor. J Biotechnol 164: 318–329
5. Blaby IK, Glaesener AG, Mettler T, Fitz-Gibbon ST, Gallaher SD, Liu B, Boyle NR, Kropat J, Stitt M, Johnson S, et al (2013) Systems-level analysis of nitrogen starvation-induced modifications of carbon metabolism in a Chlamydomonas reinhardtii starchless mutant. Plant Cell 25: 4305–4323
6. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911–917
7. Boyle NR, Page MD, Liu B, Blaby IK, Casero D, Kropat J, Cokus SJ, Hong-Hermesdorf A, Shaw J, Karpowicz SJ, et al (2012) Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J Biol Chem 287: 15811–15825
8. Chen GQ, Jiang Y, Chen F (2008) Salt-induced alterations in lipid composition of diatom Nitzschia laevis (Bacillariophyceae) under heterotrophic culture condition. J Phycol 44: 1309–1314
9. Daboussi F, Leduc S, Maréchal A, Dubois G, Guyot V, Perez-Michaut C, Amato A, Falciatore A, Juillerat A, Beurdeley M, et al (2014) Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun 5: 3831
10. 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 Cell Physiol 53: 1380–1390
11. Fernández E, Llamas Á, Galván A (2009) Nitrogen assimilation and its regulation. In D Stern, EH Harris, eds, The Chlamydomonas Source Book. Vol. 2: Organellar and Metabolic Processes, Ed 2. Elsevier, Dordrecht, The Netherlands, pp 69–113
12. 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. Eukaryot Cell 10: 1592–1606
13. Guimerá J, Casas C, Pucharcòs C, Solans A, Domènech A, Planas AM, Ashley J, Lovett M, Estivill X, Pritchard MA (1996) A human homologue of Drosophila minibrain (MNB) is expressed in the neuronal regions affected in Down syndrome and maps to the critical region. Hum Mol Genet 5: 1305–1310
14. Harris EH (2009) Chlamydomonas in the laboratory. In D Stern, EH Harris, eds, The Chlamydomonas Source Book. Vol. 1: Introduction to Chlamydomonas and Its Laboratory Use, Ed 2. Elsevier, Dordrecht, The Netherlands, pp 241–302
15. Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184–1194
16. Hu HC, Wang YY, Tsay YF (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J 57: 264–278
17. Iwai M, Ikeda K, Shimojima M, Ohta H (2014) Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type-2 diacylglycerol acyltransferase with a phosphorus starvation-inducible promoter. Plant Biotechnol J 12: 808–819
18. Izumo A, Fujiwara S, Oyama Y, Satoh A, Fujita N, Nakamura Y, Tsuzuki M (2007) Physicochemical properties of starch in Chlorella change depending on the CO2 concentration during growth: comparison of structure and properties of pyrenoid and stroma starch. Plant Sci 172: 1138–1147
19. Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4: 18
20. Johnson X, Alric J (2013) Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot Cell 12: 776–793
21. Kajikawa M, Yamato KT, Kohzu Y, Shoji S, Matsui K, Tanaka Y, Sakai Y, Fukuzawa H (2006) A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by v13 desaturation in methylotrophic yeast and tobacco. Plant Cell Physiol 47: 64–73
22. Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P (2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. Proc Natl Acad Sci USA 98: 4238–4242
23. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25
24. Lee P, Cho BR, Joo HS, Hahn JS (2008) Yeast Yak1 kinase, a bridge between PKA and stress-responsive transcription factors, Hsf1 and Msn2/ Msn4. Mol Microbiol 70: 882–895
25. 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
26. Li Y, Han D, Hu G, Dauvillee D, Sommerfeld M, Ball S, Hu Q (2010) Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol. Metab Eng 12: 387–391
27. Lin H, Kwan AL, Dutcher SK (2010) Synthesizing and salvaging NAD: lessons learned from Chlamydomonas reinhardtii. PLoS Genet 6: e1001105
28. Longworth J, Noirel J, Pandhal J, Wright PC, Vaidyanathan S (2012) HILIC- and SCX-based quantitative proteomics of Chlamydomonas reinhardtii during nitrogen starvation induced lipid and carbohydrate accumulation. J Proteome Res 11: 5959–5971
29. Martin DE, Soulard A, Hall MN (2004) TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119: 969–979
30. Merchant SS, Kropat J, Liu B, Shaw J, Warakanont J (2012) TAG, you’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23: 352–363
31. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245–250
32. Miller R, Wu G, Deshpande RR, Vieler A, Gärtner K, Li X, Moellering ER, Zäuner S, Cornish AJ, Liu B, et al (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154: 1737–1752
33. Moriya H, Shimizu-Yoshida Y, Omori A, Iwashita S, Katoh M, Sakai A (2001) Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev 15: 1217–1228
34. Nakazawa Y, Hiraki M, Kamiya R, Hirono M (2007) SAS-6 is a cartwheel protein that establishes the 9-fold symmetry of the centriole. Curr Biol 17: 2169–2174
35. Nordhues A, Schöttler MA, Unger AK, Geimer S, Schönfelder S, Schmollinger S, Rütgers M, Finazzi G, Soppa B, Sommer F, et al (2012) Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas. Plant Cell 24: 637–659
36. Park JJ, Wang H, Gargouri M, Deshpande RR, Skepper JN, Holguin FO, Juergens MT, Shachar-Hill Y, Hicks LM, Gang DR (2015) The response of Chlamydomonas reinhardtii to nitrogen deprivation: a systems biology analysis. Plant J 81: 611–624
37. Pérez-Martín M, Pérez-Pérez ME, Lemaire SD, Crespo JL (2014) Oxidative stress contributes to autophagy induction in response to endoplasmic reticulum stress in Chlamydomonas reinhardtii. Plant Physiol 166: 997–1008
38. Riekhof WR, Benning C (2009) Glycerolipids biosynthesis. In D Stern, EH Harris, eds, The Chlamydomonas Source Book. Vol. 2: Organellar and Metabolic Processes, Ed 2. Elsevier, Dordrecht, The Netherlands, pp 41–68
39. 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. Eukaryot Cell 13: 256–266
40. Sato A, Matsumura R, Hoshino N, Tsuzuki M, Sato N (2014) Responsibility of regulatory gene expression and repressed protein synthesis for triacylglycerol accumulation on sulfur-starvation in Chlamydomonas reinhardtii. Front Plant Sci 5: 444
41. Schmollinger S, Mühlhaus T, Boyle NR, Blaby IK, Casero D, Mettler T, Moseley JL, Kropat J, Sommer F, Strenkert D, et al (2014) Nitrogensparing mechanisms in Chlamydomonas affect the transcriptome, the proteome, and photosynthetic metabolism. Plant Cell 26: 1410–1435
42. Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, 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
43. Spalding MH (2009) The CO2-concentrating mechanism and carbon assimilation. In D Stern, EH Harris, eds, The Chlamydomonas Source Book. Vol. 2: Organellar and Metabolic Processes, Ed 2. Elsevier, Dordrecht, The Netherlands, pp 257–301
44. Vallon O, Spalding MH (2009) Amino acid metabolism. In D Stern, EH Harris, eds, The Chlamydomonas Source Book. Vol. 2: Organellar and Metabolic Processes, Ed 2. Elsevier, Dordrecht, The Netherlands, pp 115–158
45. Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40: 725–732
46. Wang L, Yamano T, Kajikawa M, Hirono M, Fukuzawa H (2014) Isolation and characterization of novel high-CO2-requiring mutants of Chlamydomonas reinhardtii. Photosynth Res 121: 175–184
47. Wei L, Derrien B, Gautier A, Houille-Vernes L, Boulouis A, Saint-Marcoux D, Malnoë A, Rappaport F, de Vitry C, Vallon O, et al (2014) Nitric oxidetriggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26: 353–372
48. Wintermans JF, de Mots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochim Biophys Acta 109: 448–453
49. 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. Eukaryot Cell 9: 1251–1261
50. Yamano T, Iguchi H, Fukuzawa H (2013) Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal. J Biosci Bioeng 115: 691–694
51. Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147: 340–354
52. Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid:diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24: 3708–3724
53. Yoshida K (2008) Role for DYRK family kinases on regulation of apoptosis. Biochem Pharmacol 76: 1389–1394
54. Zhang JQ, He GJ, Yan YB (2013) Biochemical and biophysical characterization of the deadenylase CrCaf1 from Chlamydomonas reinhardtii. PLoS ONE 8: e69582