Use of 1H nuclear magnetic resonance to measure intracellular metabolite levels during growth and asexual sporulation in Neurospora crassa

Eukaryotic Cell

Volumn 10, Issue 6, 2011, Pages 820-831

  Kim, James D ^a   Kaiser, Kayla ^a   Larive, Cynthia K ^a   Borkovich, Katherine A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; NEUROSPORA CRASSA;

ADENOSINE; ALLANTOIN; AMINO ACID; CHOLINE; FUMARIC ACID DERIVATIVE; FUNGAL PROTEIN; GLUCOSE; MANNITOL; SUCROSE; TREHALOSE;

ARTICLE; CULTURE MEDIUM; FUNGUS SPORE; GENE INACTIVATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOME; METABOLOMICS; METHODOLOGY; NEUROSPORA CRASSA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS;

ADENOSINE; ALLANTOIN; AMINO ACIDS; CHOLINE; CULTURE MEDIA; FUMARATES; FUNGAL PROTEINS; GENE KNOCKOUT TECHNIQUES; GLUCOSE; MAGNETIC RESONANCE SPECTROSCOPY; MANNITOL; METABOLOME; METABOLOMICS; NEUROSPORA CRASSA; PRINCIPAL COMPONENT ANALYSIS; SPORES, FUNGAL; SUCROSE; TRANSCRIPTION, GENETIC; TREHALOSE;

EID: 79957939460     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00231-10     Document Type: Article

References (74)

1. Abelson, P. H., and H. J. Vogel. 1954. Amino acid biosynthesis in Torulopsis utilis and Neurospora crassa. J. Biol. Chem. 213:355-364.
2. Boernsen, K. O., S. Gatzek, and G. Imbert. 2005. Controlled protein precipitation in combination with chip-based nanospray infusion mass spectrometry. An approach for metabolomics profiling of plasma. Anal. Chem. 77:7255-7264.
3. Borkovich, K. A., et al. 2004. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol. Mol. Biol. Rev. 68:1-108.
4. Brambl, R. 1975. Presence of polyribosomes in conidiospores of Botryodiplodia theobromae harvested with nonaqueous solvents. J. Bacteriol. 122: 1394-1395.
5. Branco-Price, C., K. A. Kaiser, C. J. H. Jang, C. K. Larive, and J. Bailey- Serres. 2008. Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 56:743-755.
6. Broadhurst, D. I., and D. B. Kell. 2006. Statistical strategies for avoiding false discoveries in metabolomics and related experiments. Metabolomics 2:171-196.
7. Brown, J. K. M., and M. S. Hovmoller. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537-541.
8. Carollo, C. A., et al. 2010. Fungal tyrosine betaine, a novel secondary metabolite from conidia of entomopathogenic Metarhizium spp. fungi. Fungal Biol. 114:473-480.
9. Christensen, R. L., and J. C. Schmit. 1980. Regulation and glutamic acid decarboxylase during Neurospora crassa conidial germination. J. Bacteriol. 144:983-990.
10. Colot, H. V., et al. 2006. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc. Natl. Acad. Sci. U. S. A. 103:10352-10357.
11. Colvin, H. J., B. L. Sauer, and K. D. Munkres. 1973. Glucose utilization and ethanolic fermentation by wild type and extrachromosomal mutants of Neurospora crassa. J. Bacteriol. 116:1322-1328.
12. Cooper, T. G., V. T. Chisholm, H. J. Cho, and H. S. Yoo. 1987. Allantoin transport in Saccharomyces cerevisiae is regulated by two induction systems. J. Bacteriol. 169:4660-4667.
13. Cossins, E. A., S. H. Y. Pang, and P. Y. Chan. 1980. Glycine synthesis in a Neurospora mutant deficient in serine hydroxymethyltransferase. Plant Cell Physiol. 21:719-729.
14. Cui, Q., et al. 2008. Metabolite identification via the Madison Metabolomics Consortium Database. Nat. Biotech. 26:162-164.
15. Davis, R. H. 2000. Neurospora: contributions of a model organism. Oxford University Press, New York, NY.
16. Davis, R. H. 2010. Amino acids and polyamines: polyfunctional proteins, metabolic cycles, and compartmentation, p. 339-358. In K. A. Borkovich and D. J. Ebbole (ed.), Cellular and molecular biology of filamentous fungi. ASM press, Washington, DC.
17. Davis, R. H., F. J. de Serres, H. Tabor, and C. W. Tabor. 1970. Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol. 17:79-143.
18. d'Enfert, C., B. M. Bonini, P. D. A. Zapella, T. Fontaine, A. M. da Silva, and H. F. Terenzi. 1999. Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa. Mol. Microbiol. 32:471-483.
19. d'Enfert, C., and T. Fontaine. 1997. Molecular characterization of the Aspergillus nidulans treA gene encoding an acid trehalase required for growth on trehalose. Mol. Microbiol. 24:203-216.
20. de Pinho, C. A., M. de Lourdes, T. M. Polizeli, J. A. Jorge, and H. F. Terenzi. 2001. Mobilisation of trehalose in mutants of the cyclic AMP signaling pathway, cr-1 (CRISP-1) and mcb (microcycle conidiation), of Neurospora crassa. FEMS Microbiol. Lett. 199:85-89.
21. Dieterle, F., A. Ross, G. Schlotterbeck, and H. Senn. 2006. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics. Anal. Chem. 78:4281-4290.
22. Elbein, A. D., Y. T. Pan, I. Pastuszak, and D. Carroll. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R-27R.
23. Fiehn, O., et al. 2000. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 18:1157-1161.
24. Halsall, D. M., and D. E. Catcheside. 1971. Structural genes for DAHP synthase isoenzymes in Neurospora crassa. Genetics 67:183-188.
25. Halsall, D. M., D. E. Catcheside, and C. H. Doy. 1971. Some properties of the 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase isoenzymes from mutant strains of Neurospora crassa. Biochim. Biophys. Acta 227:464-472.
26. Halsall, D. M., and C. H. Doy. 1969. Studies concerning the biochemical genetics and physiology of activity and allosteric inhibition mutants of Neurospora crassa 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase. Biochim. Biophys. Acta 185:432-446.
27. Hill, E. P., and A. S. Sussman. 1964. Development of trehalase and invertase activity in Neurospora. J. Bacteriol. 88:1556-1566.
28. Hogg, J. A., and M. Richardson. 1968. Biosynthesis of betaine in Neurospora crassa. Arch. Mikrobiol. 62:153-156.
29. Horikoshi, K., and Y. Ikeda. 1966. Trehalase in conidia of Aspergillus oryzae. J. Bacteriol. 91:1883-1887.
30. Horne, D. W., and H. P. Broquist. 1973. Role of lysine and N-trimethyllysine in carnitine biosynthesis. I. Studies in Neurospora crassa. J. Biol. Chem. 248:2170-2175.
31. Jewett, M. C., G. Hofmann, and J. Nielsen. 2006. Fungal metabolite analysis in genomics and phenomics. Curr. Opin. Biotechnol. 17:191-197.
32. Kaiser, K. A., G. A. Barding, and C. K. Larive. 2009. Metabolic profiling of plants by 1H-NMR: a comparison of metabolite extraction strategies using rosette leaves of the model plant Arabidopsis thaliana. Magn. Reson. Chem. 47:S147-S156.
33. Kaiser, K. A., C. E. Merrywell, F. Fang, and C. K. Larive. 2008. Metabolic profiling, p. 233-267. In I. Wawer, U. Holzgrabe, and B. Diehl (ed.), NMR spectroscopy in pharmaceutical analysis. Elsevier, Oxford, United Kingdom.
34. Kanamori, K., T. L. Legerton, R. L. Weiss, and J. D. Roberts. 1982. Effect of the nitrogen source on glutamine and alanine biosynthesis in Neurospora crassa. An in vivo 15N nuclear magnetic resonance study. J. Biol. Chem. 257:14168-14172.
35. Kasuga, T., et al. 2005. Long-oligomer microarray profiling in Neurospora crassa reveals the transcriptional program underlying biochemical and physiological events of conidial germination. Nucleic Acids Res. 33:6469-6485.
36. Kays, A. M., and K. A. Borkovich. 2004. Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics 166:1229-1240.
37. Kays, A. M., P. S. Rowley, R. A. Baasiri, and K. A. Borkovich. 2000. Regulation of conidiation and adenylyl cyclase levels by the G-alpha protein GNA-3 in Neurospora crassa. Mol. Cell. Biol. 20:7693-7705.
38. Koelle, M. R. 2006. Heterotrimeric G protein signaling: getting inside the cell. Cell 126:25-27.
39. Kuepfer, L., U. Sauer, and L. M. Blank. 2005. Metabolic functions of duplicate genes in Saccharomyces cerevisiae. Genome Res. 15:1421-1430.
40. Lerch, K. 1981. Metal ions in biological systems, vol. 13. Marcel Dekker, Inc., New York, NY.
41. Li, L., and K. A. Borkovich. 2006. GPR-4 is a Predicted G-protein-coupled receptor required for carbon source-dependent asexual growth and development in Neurospora crassa. Eukaryot. Cell 5:1287-1300.
42. Li, L., S. J. Wright, S. Krystofova, G. Park, and K. A. Borkovich. 2007. Heterotrimeric G protein signaling in filamentous fungi. Annu. Rev. Microbiol. 61:423-452.
43. Lin, C. Y., H. F. Wu, R. S. Tjeerdema, and M. R. Viant. 2007. Evaluation of metabolite extraction strategies from tissue samples using NMR metabolomics. Metabolomics 3:55-67.
44. Linden, H., P. Ballario, and G. Macino. 1997. Blue light regulation in Neurospora crassa. Fungal Genet. Biol. 22:141-150.
45. Lindon, J. C., E. Holmes, and J. K. Nicholson. 2003. So what's the deal with metabonomics? Anal. Chem. 75:384A-391A.
46. Lowe, R. G., et al. 2010. A combined (1)H nuclear magnetic resonance and electrospray ionization-mass spectrometry analysis to understand the basal metabolism of plant-pathogenic Fusarium spp. Mol. Plant Microbe Interact. 23:1605-1618.
47. Martin, F. P., et al. 2007. A top-down systems biology view of microbiomemammalian metabolic interactions in a mouse model. Mol. Syst. Biol. 3:112.
48. Marzluf, G. 1997. Genetic regulation of nitrogen metabolism in the fungi. Microbiol. Mol. Biol. Rev. 61:17-32.
49. Munkres, K. D. 1968. Genetic and epigenetic forms of malate dehydrogenase in Neurospora. Ann. N. Y. Acad. Sci. 151:294-306.
50. Orbach, M. J., M. S. Sachs, and C. Yanofsky. 1990. The Neurospora crassa arg-2 locus. Structure and expression of the gene encoding the small subunit of arginine-specific carbamoyl phosphate synthetase. J. Biol. Chem. 265: 10981-10987.
51. Pall, M. L. 1981. Adenosine 3 ́,5 ́-phosphate in fungi. Microbiol. Rev. 45: 462-480.
52. Pall, M. L., and C. K. Robertson. 1988. Regulation of lactate/pyruvate ratios by cyclic AMP in Neurospora crassa. Biochem. Biophys. Res. Commun. 150:365-370.
53. Perkins, D. D., A. Radford, and M. S. Sachs. 2001. The Neurospora compendium: chromosomal loci. Academic Press, San Diego, CA.
54. Pillonel, C., and T. Meyer. 1997. Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pestic. Sci. 49: 229-236.
55. Plesofsky-vig, N., D. Light, and R. Brambl. 1983. Paedogenetic conidiation in Neurospora crassa. Exp. Mycol. 7:283-286.
56. Plesofsky, N., and R. Brambl. 1999. Glucose metabolism in Neurospora is altered by heat shock and by disruption of HSP30. Biochim. Biophys. Acta 1449:73-82.
57. Radford, A. 2004. Metabolic highways of Neurospora crassa revisited. Adv. Genet. 52:165-207.
58. Ringner, M. 2008. What is principal component analysis? Nat. Biotechnol. 26:303-304.
59. Robertson, D. G. 2005. Metabonomics in toxicology: a review. Toxicol. Sci. 85:809-822.
60. Sachs, M. S., and C. Yanofsky. 1991. Developmental expression of genes involved in conidiation and amino acid biosynthesis in Neurospora crassa. Dev. Biol. 148:117-128.
61. Schmit, J. C., and S. Brody. 1975. Neurospora crassa conidial germination: role of endogenous amino acid pools. J. Bacteriol. 124:232-242.
62. Schmit, J. C., and S. Brody. 1976. Biochemical genetics of Neurospora crassa conidial germination. Bacteriol. Rev. 40:1-41.
63. Solomon, P. S., O. D. C. Waters, C. I. Jörgens, R. G. T. Lowe, J. Rechberger, R. D. Trengove, and R. P. Oliver. 2006. Mannitol is required for asexual sporulation in the wheat pathogen Stagonospora nodorum (glume blotch). Biochem. J. 399:231-239.
64. Solomon, P. S., O. D. C. Waters, and R. P. Oliver. 2007. Decoding the mannitol enigma in filamentous fungi. Trends Microbiol. 15:257-262.
65. Springer, M. L. 1993. Genetic control of fungal differentiation: the three sporulation pathways of Neurospora crassa. Bioessays 15:365-374.
66. Springer, M. L., and C. Yanofsky. 1989. A morphological and genetic analysis of conidiophore development in Neurospora crassa. Genes Dev. 3:559-571.
67. That, T. C., and G. Turian. 1978. Ultrastructural study of microcyclic macroconidiation in Neurospora crassa. Arch. Microbiol. 116:279-288.
68. Turian, G., and D. E. Bianchi. 1972. Conidiation in Neurospora. Bot. Rev. 38:119-154.
69. Turner, G. E., and R. L. Weiss. 2006. Developmental expression of two forms of arginase in Neurospora crassa. Biochim. Biophys. Acta 1760:848-857.
70. van den Berg, R. A., H. C. Hoefsloot, J. A. Westerhuis, A. K. Smilde, and M. J. van der Werf. 2006. Centering, scaling, and transformations: improving the biological information content of metabolomics data. BMC Genomics 7:142.
71. Viant, M. R., E. S. Rosenblum, and R. S. Tieerdema. 2003. NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism health. Environ. Sci. Technol. 37:4982-4989.
72. Villas-Boas, S. G., J. Hojer-Pedersen, M. Akesson, J. Smedsgaard, and J. Nielsen. 2005. Global metabolite analysis of yeast: evaluation of sample preparation methods. Yeast 22:1155-1169.
73. Ward, J. L., J. M. Baker, and M. H. Beale. 2007. Recent applications of NMR spectroscopy in plant metabolomics. FEBS J. 274:1126-1131
74. Zhang, S., et al. 2009. Interdependence of signal processing and analysis of urine 1H NMR spectra for metabolic profiling. Anal. Chem. 81:6080-6088.