Differential impact of nutrition on developmental and metabolic gene expression during fruiting body development in Neurospora crassa.

Zheng Wang, Nina Lehr, Frances Trail, Jeffrey P Townsend
Author Information
  1. Zheng Wang: Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, USA.

Abstract

Fungal fruiting body size and form are influenced by the ecology of the species, including diverse environmental stimuli. Accordingly, nutritional resources available to the fungus during development can be vital to successful production of fruiting bodies. To investigate the effect of nutrition, perithecial development of Neurospora crassa was induced on two different media, a chemically sparsely nutritive Synthetic Crossing Medium (SCM) and a natural Carrot Agar (CA). Protoperithecia were collected before crossing, and perithecia were collected at 2, 24, 48, 72, 96, 120, and at full maturity 144 h after crossing. No differences in fruiting body morphology were observed between the two media at any time point. A circuit of microarray hybridizations comparing cDNA from all neighboring stages was performed. For a majority of differentially expressed genes, expression was higher in SCM than in CA, and expression of core metabolic genes was particularly affected. Effects of nutrition were highest in magnitude before crossing, lowering in magnitude during early perithecial development. Interestingly, metabolic effects of the media were also large in magnitude during late perithecial development, at which stage the lower expression in CA presumably reflected the continued intake of diverse complex initial compounds, diminishing the need for expression of anabolic pathways. However, for genes with key regulatory roles in sexual development, including pheromone precursor ccg-4 and poi2, expression patterns were similar between treatments. When possible, a common nutritional environment is ideal for comparing transcriptional profiles between different fungi. Nevertheless, the observed consistency of the developmental program across media, despite considerable metabolic differentiation is reassuring. This result facilitates comparative studies that will require different nutritional resources for sexual development in different fungi.

References

  1. J Biosci. 2010 Mar;35(1):119-26 [PMID: 20413916]
  2. Fungal Genet Biol. 2003 Dec;40(3):225-33 [PMID: 14599890]
  3. Nucleic Acids Res. 2005 Nov 14;33(20):6469-85 [PMID: 16287898]
  4. Genetics. 2010 Dec;186(4):1217-30 [PMID: 20876563]
  5. Curr Biol. 2009 Sep 29;19(18):R840-5 [PMID: 19788875]
  6. Eukaryot Cell. 2006 Mar;5(3):544-54 [PMID: 16524909]
  7. Genetics. 1988 Mar;118(3):417-23 [PMID: 17246415]
  8. Nat Methods. 2008 Jul;5(7):621-8 [PMID: 18516045]
  9. Genes Dev. 1992 Jun;6(6):1052-7 [PMID: 1534304]
  10. Nucleic Acids Res. 2000 Jan 1;28(1):27-30 [PMID: 10592173]
  11. Curr Genet. 1996 Apr;29(5):490-5 [PMID: 8625430]
  12. Bioinformatics. 2011 Sep 1;27(17):2455-6 [PMID: 21712247]
  13. Mol Biol Evol. 2003 Jun;20(6):955-63 [PMID: 12716989]
  14. Proc Natl Acad Sci U S A. 1941 Nov 15;27(11):499-506 [PMID: 16588492]
  15. PLoS Biol. 2008 Dec 23;6(12):2817-30 [PMID: 19108609]
  16. PLoS One. 2011;6(9):e25654 [PMID: 21980519]
  17. Nucleic Acids Res. 2004 Oct 14;32(18):5539-45 [PMID: 15486203]
  18. Genome Biol. 2002;3(12):RESEARCH0071 [PMID: 12537560]
  19. FEMS Microbiol Lett. 2001 Nov 13;204(2):311-6 [PMID: 11731141]
  20. Fungal Genet Biol. 2007 Nov;44(11):1146-56 [PMID: 17555994]
  21. Bioinformatics. 2010 Aug 1;26(15):1918-9 [PMID: 20538728]
  22. PLoS One. 2009;4(1):e4246 [PMID: 19158947]
  23. J Biol Chem. 2000 Nov 10;275(45):34867-72 [PMID: 10956664]
  24. BMC Bioinformatics. 2004 May 05;5:54 [PMID: 15128431]
  25. Eukaryot Cell. 2003 Feb;2(1):1-8 [PMID: 12582117]
  26. Mol Cell Biol. 1990 Oct;10(10):5064-70 [PMID: 2144609]
  27. Microbiol Mol Biol Rev. 2004 Mar;68(1):1-108 [PMID: 15007097]
  28. Eukaryot Cell. 2007 Dec;6(12):2311-22 [PMID: 17951513]
  29. Bioinformatics. 2009 May 1;25(9):1105-11 [PMID: 19289445]
  30. Eukaryot Cell. 2008 Sep;7(9):1549-64 [PMID: 18676954]
  31. Fungal Genet Biol. 2010 Mar;47(3):199-204 [PMID: 20025988]
  32. BMC Genomics. 2010 Aug 17;11:477 [PMID: 20716356]
  33. IMA Fungus. 2011 Jun;2(1):81-6 [PMID: 22679591]
  34. J Biol Chem. 2000 Oct 13;275(41):31555-8 [PMID: 10934218]
  35. Eukaryot Cell. 2005 May;4(5):900-10 [PMID: 15879524]
  36. Mycol Res. 2003 Jul;107(Pt 7):861-71 [PMID: 12967214]
  37. Trends Ecol Evol. 2009 Dec;24(12):649-58 [PMID: 19699549]

Grants

  1. P01 GM068087/NIGMS NIH HHS
  2. P01 GM068067/NIGMS NIH HHS

MeSH Term

Culture Media
DNA, Complementary
DNA, Fungal
Fruiting Bodies, Fungal
Gene Expression Profiling
Gene Expression Regulation, Fungal
Metabolic Networks and Pathways
Microarray Analysis
Neurospora crassa
Time Factors

Chemicals

Culture Media
DNA, Complementary
DNA, Fungal

Word Cloud

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