Comparative transcriptome analysis reveals multiple functions for Mhy1p in lipid biosynthesis in the oleaginous yeast Yarrowia lipolytica

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1863, Issue 1, 2018, Pages 81-90

  Wang, Guangyuan ^a   Li, Delong ^a   Miao, Zhengang ^a   Zhang, Shanshan ^a   Liang, Wenxing ^a   Liu, Lin ^a  

^a QINGDAO AGRICULTURAL UNIVERSITY   (China)

Author keywords

Lipid biosynthesis; Mhy1p; Oleaginous yeast; RNA seq; Yarrowia lipolytica

Indexed keywords

ACETYL COENZYME A; AMINO ACID; AMMONIA; CARBON; CITRIC ACID; NITROGEN; TRIACYLGLYCEROL; UNSATURATED FATTY ACID; URACIL; BIO-OIL; DNA BINDING PROTEIN; FUNGAL PROTEIN; LIPID; MHY1 PROTEIN, YARROWIA LIPOLYTICA; POLYPHENOL; TRANSCRIPTOME; VEGETABLE OIL;

AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; ARTICLE; CELL CYCLE REGULATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRY WEIGHT; FUNGAL GENE; FUNGUS GROWTH; GENE EXPRESSION; GENE FUNCTION; GENE INACTIVATION; LIPOGENESIS; MHY1P GENE; NITROGEN METABOLISM; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTOMICS; YARROWIA LIPOLYTICA; BIOSYNTHESIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; TRANSGENIC ORGANISM; YARROWIA;

DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; LIPID METABOLISM; LIPIDS; LIPOGENESIS; METABOLIC NETWORKS AND PATHWAYS; ORGANISMS, GENETICALLY MODIFIED; PLANT OILS; POLYPHENOLS; TRANSCRIPTOME; YARROWIA;

EID: 85032385837     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2017.10.003     Document Type: Article

References (60)

1. Papanikolaou, S., Aggelis, G., Modeling lipid accumulation and degradation in Yarrowia lipolytica cultivated on industrial fats. Curr. Microbiol. 46 (2003), 398–402.
2. Sitepu, I.R., Garay, L.A., Sestric, R., Levin, D., Block, D.E., German, J.B., Boundy-Mills, K.L., Oleaginous yeasts for biodiesel: current and future trends in biology and production. Biotechnol. Adv. 32 (2014), 1336–1360.
3. Wang, Z., Fu, W., Xu, H., Chi, Z., Direct conversion of inulin into cell lipid by an inulinase-producing yeast Rhodosporidium toruloides 2F5. Bioresour. Technol. 161 (2014), 131–136.
4. Ageitos, J.M., Vallejo, J.A., Veiga-Crespo, P., Villa, T.G., Oily yeasts as oleaginous cell factories. Appl. Microbiol. Biotechnol. 90 (2011), 1219–1227.
5. Wang, Z.P., Xu, H.M., Wang, G.Y., Chi, Z., Chi, Z.M., Disruption of the MIG1 gene enhances lipid biosynthesis in the oleaginous yeast Yarrowia lipolytica ACA-DC 50109. Biochim. Biophys. Acta 1831 (2013), 675–682.
6. Beopoulos, A., Nicaud, J.M., Gaillardin, C., An overview of lipid metabolism in yeasts and its impact on biotechnological processes. Appl. Microbiol. Biotechnol. 90 (2011), 1193–1206.
7. Beopoulos, A., Cescut, J., Haddouche, R., Uribelarrea, J.L., Molinajouve, C., Nicaud, J.M., Yarrowia lipolytica as a model for bio-oil production. Prog. Lipid Res. 48 (2009), 375–387.
8. Dulermo, T., Lazar, Z., Dulermo, R., Rakicka, M., Haddouche, R., Nicaud, J.M., Analysis of ATP-citrate lyase and malic enzyme mutants of Yarrowia lipolytica points out the importance of mannitol metabolism in fatty acid synthesis. Biochim. Biophys. Acta 1851 (2015), 1107–1117.
9. Seip, J., Jackson, R., He, H., Zhu, Q., Hong, S.P., Snf1 is a regulator of lipid accumulation in Yarrowia lipolytica. Appl. Environ. Microbiol. 79 (2013), 7360–7370.
10. Dulermo, T., Treton, B., Beopoulos, A., Gnankon, A.P.K., Haddouche, R., Nicaud, J., Characterization of the two intracellular lipases of Y. lipolytica encoded by TGL3 and TGL4 genes: new insights into the role of intracellular lipases and lipid body organisation. Biochim. Biophys. Acta 1831 (2013), 1486–1495.
11. Liu, L., Markham, K., Blazeck, J., Zhou, N., Leon, D., Otoupal, P., Alper, H.S., Surveying the lipogenesis landscape in Yarrowia lipolytica through understanding the function of a Mga2p regulatory protein mutant. Metab. Eng. 31 (2015), 102–111.
12. Pomraning, K.R., Bredeweg, E.L., Baker, S.E., Regulation of nitrogen metabolism by GATA zinc finger transcription factors in Yarrowia lipolytica. mSphere, 2, 2017, e00038-17.
13. Liang, S.H., Wu, H., Wang, R.R., Wang, Q., Shu, T., Gao, X.D., The TORC1-Sch9-Rim15 signaling pathway represses yeast-to-hypha transition in response to glycerol availability in the oleaginous yeast Yarrowia lipolytica. Mol. Microbiol. 104 (2017), 553–567.
14. Ota, Y., Oikawa, S., Morimoto, Y., Minoda, Y., Nutritional factors causing mycelial development of Saccharomycopsis lipolytica. Agric. Biol. Chem. 48 (1984), 1933–1939.
15. Novotny, C., Dolezalova, L., Lieblova, J., Dimorphic growth and lipase production in lipolytic yeasts. Folia Microbiol. 39 (1994), 71–73.
16. 2-type zinc finger protein that promotes dimorphic transition in the yeast Yarrowia lipolytica. J. Bacteriol. 181 (1999), 3051–3057.
17. 2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12 (1998), 586–597.
18. Papanikolaou, S., Aggelis, G., Lipids of oleaginous yeasts. Part I: biochemistry of single cell oil production. Eur. J. Lipid Sci. Technol. 113 (2011), 1031–1051.
19. Zhu, Z., Zhang, S., Liu, H., Shen, H., Lin, X., Yang, F., Zhou, Y.J., Jin, G., Ye, M., Zou, H., Zhao, Z.K., A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat. Commun., 3, 2012, 1112.
20. Papanikolaou, S., Aggelis, G., Selective uptake of fatty acids by the yeast Yarrowia lipolytica. Eur. J. Lipid Sci. Technol. 105 (2003), 651–655.
21. Wang, G.Y., Zhang, Y., Chi, Z., Liu, G.L., Wang, Z.P., Chi, Z.M., Role of pyruvate carboxylase in accumulation of intracellular lipid of the oleaginous yeast Yarrowia lipolytica ACA-DC 50109. Appl. Microbiol. Biotechnol. 99 (2015), 1637–1645.
22. Wang, G., Guo, L., Liang, W., Chi, Z., Liu, L., Systematic analysis of the lysine acetylome reveals diverse functions of lysine acetylation in the oleaginous yeast Yarrowia lipolytica. AMB Express, 7, 2017, 94.
23. Wang, F., Yue, L., Wang, L., Madzak, C., Li, J., Wang, X., Chi, Z., Genetic modification of the marine-derived yeast Yarrowia lipolytica with high-protein content using a GPI-anchor-fusion expression system. Biotechnol. Prog. 25 (2009), 1297–1303.
24. Xuan, J.W., Fournier, P., Gaillardin, C., Cloning of the LYS5 gene encoding saccharopine dehydrogenase from the yeast Yarrowia lipolytica by target integration. Curr. Genet. 14 (1988), 15–21.
25. Camp, B.J., Farmer, L., A rapid spectrophotometric method for the determination of citric acid in blood. Clin. Chem. 13 (1967), 501–505.
26. Wang, C.L., Yang, L., Xin, F.H., Liu, Y.Y., Chi, Z.M., Evaluation of single cell oil from Aureobasidium pullulans var. melanogenum P10 isolated from mangrove ecosystems for biodiesel production. Process Biochem. 49 (2014), 725–731.
27. Trapnell, C., Pachter, L., Salzberg, S.L., TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 (2009), 1105–1111.
28. Anders, S., Pyl, P.T., Huber, W., HTSeq — a python framework to work with high-throughput sequencing data. Bioinformatics 31 (2015), 166–169.
29. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 (2010), 511–515.
30. Wang, L., Feng, Z., Wang, X., Wang, X., Zhang, X., DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26 (2010), 136–138.
31. Couto, N., Belas, A., Oliveira, M., Almeida, P., Clemente, C., Pomba, C., Comparative RNA-seq-based transcriptome analysis of the virulence characteristics of methicillin-resistant and -susceptible Staphylococcus pseudintermedius strains isolated from small animals. Antimicrob. Agents Chemother. 60 (2016), 962–967.
32. Young, M.D., Wakefield, M.J., Smyth, G.K., Oshlack, A., Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol., 11, 2010, R14.
33. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S., Tokimatsu, T., Yamanishi, Y., KEGG for linking genomes to life and the environment. Nucleic Acids Res. 36 (2008), D480–484.
34. Livak, K.J., Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2(− delta delta C(T)) Method. Methods 25 (2001), 402–408.
35. Athenstaedt, K., Daum, G., The life cycle of neutral lipids: synthesis, storage and degradation. Cell. Mol. Life Sci. 63 (2006), 1355–1369.
36. Czabany, T., Athenstaedt, K., Daum, G., Synthesis, storage and degradation of neutral lipids in yeast. Biochim. Biophys. Acta 1771 (2007), 299–309.
37. Ratledge, C., Wynn, J.P., The biochemistry and molecular biology of lipid accumulation in oleaginous microorganisms. Adv. Appl. Microbiol. 51 (2002), 1–51.
38. Kerkhoven, E.J., Pomraning, K.R., Baker, S.E., Nielsen, J., Regulation of amino-acid metabolism controls flux to lipid accumulation in Yarrowia lipolytica. NPJ Syst. Biol. Appl., 2, 2016, 16005.
39. Dulermo, T., Nicaud, J., Involvement of the G3P shuttle and β-oxidation pathway in the control of TAG synthesis and lipid accumulation in Yarrowia lipolytica. Metab. Eng. 13 (2011), 482–491.
40. Blazeck, J., Hill, A., Liu, L., Knight, R., Miller, J., Pan, A., Otoupal, P., Alper, H.S., Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production. Nat. Commun., 5, 2014, 3131.
41. Qiao, K., Abidi, S.H.I., Liu, H., Zhang, H., Chakraborty, S., Watson, N., Ajikumar, P.K., Stephanopoulos, G., Engineering lipid overproduction in the oleaginous yeast Yarrowia lipolytica. Metab. Eng. 29 (2015), 56–65.
42. Fakas, S., Lipid biosynthesis in yeasts: a comparison of the lipid biosynthetic pathway between the model non-oleaginous yeast Saccharomyces cerevisiae and the model oleaginous yeast Yarrowia lipolytica. Eng. Life Sci. 17 (2017), 292–302.
43. Seidl, V., Seiboth, B., Karaffa, L., Kubicek, C.P., The fungal STRE-element-binding protein Seb1 is involved but not essential for glycerol dehydrogenase (gld1) gene expression and glycerol accumulation in Trichoderma atroviride during osmotic stress. Fungal Genet. Biol. 41 (2004), 1132–1140.
44. Kahana-Edwin, S., Stark, M., Kassir, Y., Multiple MAPK cascades regulate the transcription of IME1, the master transcriptional activator of meiosis in Saccharomyces cerevisiae. PLoS One, 8, 2013, e78920.
45. Kassir, Y., Granot, D., Simchen, G., IME1, a positive regulator gene of meiosis in S. cerevisiae. Cell 52 (1988), 853–862.
46. Beck, T., Hall, M.N., The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402 (1999), 689–692.
47. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J.L., Bonenfant, D., Oppliger, W., Jenoe, P., Hall, M.N., Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10 (2002), 457–468.
48. Rohde, J.R., Heitman, J., Cardenas, M.E., The TOR kinases link nutrient sensing to cell growth. J. Biol. Chem. 276 (2001), 9583–9586.
49. Imamura, S., Kawase, Y., Kobayashi, I., Sone, T., Era, A., Miyagishima, S.Y., Shimojima, M., Ohta, H., Tanaka, K., Target of rapamycin (TOR) plays a critical role in triacylglycerol accumulation in microalgae. Plant Mol. Biol. 89 (2015), 309–318.
50. Imamura, S., Kawase, Y., Kobayashi, I., Shimojima, M., Ohta, H., Tanaka, K., TOR (target of rapamycin) is a key regulator of triacylglycerol accumulation in microalgae. Plant Signal. Behav., 11, 2016, e1149285.
51. Madeira, J.B., Masuda, C.A., Mayamonteiro, C.M., Matos, G., Monterolomeli, M., Bozaquelmorais, B.L., TORC1 inhibition induces lipid droplet replenishment in yeast. Mol. Cell. Biol. 35 (2015), 737–746.
52. Laplante, M., Sabatini, D.M., An emerging role of mTOR in lipid biosynthesis. Curr. Biol. 19 (2009), R1046–R1052.
53. Kersten, S., Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep. 2 (2001), 282–286.
54. Yuan, W., Guo, S., Gao, J., Zhong, M., Yan, G., Wu, W., Chao, Y., Jiang, Y., General control nonderepressible 2 (GCN2) kinase inhibits target of rapamycin complex 1 in response to amino acid starvation in Saccharomyces cerevisiae. J. Biol. Chem. 292 (2017), 2660–2669.
55. Kerkhoven, E.J., Kim, Y.M., Wei, S., Nicora, C.D., Fillmore, T.L., Purvine, S.O., Webbrobertson, B.J., Smith, R.D., Baker, S.E., Metz, T.O., Leucine biosynthesis is involved in regulating high lipid accumulation in Yarrowia lipolytica. MBio, 8, 2017, e00857-17.
56. Kingsbury, J.M., Sen, N.D., Cardenas, M.E., Branched-chain aminotransferases control TORC1 signaling in Saccharomyces cerevisiae. PLoS Genet., 11, 2015, e1005714.
57. Han, J.M., Jeong, S.J., Park, M.C., Kim, G., Kwon, N.H., Kim, H.K., Ha, S.H., Ryu, S.H., Kim, S., Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway. Cell 149 (2012), 410–424.
58. Morin, N., Cescut, J., Beopoulos, A., Lelandais, G., Berre, V.L., Uribelarrea, J., Molinajouve, C., Nicaud, J., Transcriptomic analyses during the transition from biomass production to lipid accumulation in the oleaginous yeast Yarrowia lipolytica. PLoS One, 6, 2011, e27966.
59. Moretti, M.B., Batlle, A., Garcia, S.C., UGA4 gene encoding the γ-aminobutyric acid permease in Saccharomyces cerevisiae is an acid-expressed gene. Int. J. Biochem. Cell Biol. 33 (2001), 1202–1207.
60. Liu, L., Pan, A., Spofford, C., Zhou, N., Alper, H.S., An evolutionary metabolic engineering approach for enhancing lipogenesis in Yarrowia lipolytica. Metab. Eng. 29 (2015), 36–45.