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Identification of new developmentally regulated genes involved in Streptomyces coelicolor sporulation

Salerno, Paola LU ; Persson, Jessica ; Bucca, Giselda ; Laing, Emma ; Ausmees, Nora LU ; Smith, Colin P. and Flärdh, Klas LU (2013) In BMC Microbiology 13.
Abstract
Background: The sporulation of aerial hyphae of Streptomyces coelicolor is a complex developmental process. Only a limited number of the genes involved in this intriguing morphological differentiation programme are known, including some key regulatory genes. The aim of this study was to expand our knowledge of the gene repertoire involved in S. coelicolor sporulation. Results: We report a DNA microarray-based investigation of developmentally controlled gene expression in S. coelicolor. By comparing global transcription patterns of the wild-type parent and two mutants lacking key regulators of aerial hyphal sporulation, we found a total of 114 genes that had significantly different expression in at least one of the two mutants compared to... (More)
Background: The sporulation of aerial hyphae of Streptomyces coelicolor is a complex developmental process. Only a limited number of the genes involved in this intriguing morphological differentiation programme are known, including some key regulatory genes. The aim of this study was to expand our knowledge of the gene repertoire involved in S. coelicolor sporulation. Results: We report a DNA microarray-based investigation of developmentally controlled gene expression in S. coelicolor. By comparing global transcription patterns of the wild-type parent and two mutants lacking key regulators of aerial hyphal sporulation, we found a total of 114 genes that had significantly different expression in at least one of the two mutants compared to the wild-type during sporulation. A whiA mutant showed the largest effects on gene expression, while only a few genes were specifically affected by whiH mutation. Seven new sporulation loci were investigated in more detail with respect to expression patterns and mutant phenotypes. These included SCO7449-7451 that affect spore pigment biogenesis; SCO1773-1774 that encode an L-alanine dehydrogenase and a regulator-like protein and are required for maturation of spores; SCO3857 that encodes a protein highly similar to a nosiheptide resistance regulator and affects spore maturation; and four additional loci (SCO4421, SCO4157, SCO0934, SCO1195) that show developmental regulation but no overt mutant phenotype. Furthermore, we describe a new promoter-probe vector that takes advantage of the red fluorescent protein mCherry as a reporter of cell type-specific promoter activity. Conclusion: Aerial hyphal sporulation in S. coelicolor is a technically challenging process for global transcriptomic investigations since it occurs only as a small fraction of the colony biomass and is not highly synchronized. Here we show that by comparing a wild-type to mutants lacking regulators that are specifically affecting processes in aerial hypha, it is possible to identify previously unknown genes with important roles in sporulation. The transcriptomic data reported here should also serve as a basis for identification of further developmentally important genes in future functional studies. (Less)
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author
organization
publishing date
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Contribution to journal
publication status
published
subject
keywords
Differentiation, Aerial mycelium, Spore, Transcriptome, Spore pigment, Alanine dehydrogenase
in
BMC Microbiology
volume
13
article number
281
publisher
BioMed Central
external identifiers
  • wos:000330075800001
  • scopus:84888998253
  • pmid:24308424
ISSN
1471-2180
DOI
10.1186/1471-2180-13-281
language
English
LU publication?
yes
id
a4301a48-a374-42ed-941b-6367429a51a9 (old id 4319192)
date added to LUP
2016-04-01 13:46:28
date last changed
2020-01-12 13:36:43
@article{a4301a48-a374-42ed-941b-6367429a51a9,
  abstract     = {Background: The sporulation of aerial hyphae of Streptomyces coelicolor is a complex developmental process. Only a limited number of the genes involved in this intriguing morphological differentiation programme are known, including some key regulatory genes. The aim of this study was to expand our knowledge of the gene repertoire involved in S. coelicolor sporulation. Results: We report a DNA microarray-based investigation of developmentally controlled gene expression in S. coelicolor. By comparing global transcription patterns of the wild-type parent and two mutants lacking key regulators of aerial hyphal sporulation, we found a total of 114 genes that had significantly different expression in at least one of the two mutants compared to the wild-type during sporulation. A whiA mutant showed the largest effects on gene expression, while only a few genes were specifically affected by whiH mutation. Seven new sporulation loci were investigated in more detail with respect to expression patterns and mutant phenotypes. These included SCO7449-7451 that affect spore pigment biogenesis; SCO1773-1774 that encode an L-alanine dehydrogenase and a regulator-like protein and are required for maturation of spores; SCO3857 that encodes a protein highly similar to a nosiheptide resistance regulator and affects spore maturation; and four additional loci (SCO4421, SCO4157, SCO0934, SCO1195) that show developmental regulation but no overt mutant phenotype. Furthermore, we describe a new promoter-probe vector that takes advantage of the red fluorescent protein mCherry as a reporter of cell type-specific promoter activity. Conclusion: Aerial hyphal sporulation in S. coelicolor is a technically challenging process for global transcriptomic investigations since it occurs only as a small fraction of the colony biomass and is not highly synchronized. Here we show that by comparing a wild-type to mutants lacking regulators that are specifically affecting processes in aerial hypha, it is possible to identify previously unknown genes with important roles in sporulation. The transcriptomic data reported here should also serve as a basis for identification of further developmentally important genes in future functional studies.},
  author       = {Salerno, Paola and Persson, Jessica and Bucca, Giselda and Laing, Emma and Ausmees, Nora and Smith, Colin P. and Flärdh, Klas},
  issn         = {1471-2180},
  language     = {eng},
  publisher    = {BioMed Central},
  series       = {BMC Microbiology},
  title        = {Identification of new developmentally regulated genes involved in Streptomyces coelicolor sporulation},
  url          = {http://dx.doi.org/10.1186/1471-2180-13-281},
  doi          = {10.1186/1471-2180-13-281},
  volume       = {13},
  year         = {2013},
}