Novel light-regulated genes in Trichoderma atroviride: a dissection by cDNA microarrays.

The influence of light on living organisms is critical, not only because of its importance as the main source of energy for the biosphere, but also due to its capacity to induce changes in the behaviour and morphology of nearly all forms of life. The common soil fungus Trichoderma atroviride responds to blue light in a synchronized manner, in time and space, by forming a ring of green conidia at what had been the colony perimeter at the time of exposure (photoconidiation). A putative complex formed by the BLR-1 and BLR-2 proteins in T. atroviride appears to play an essential role as a sensor and transcriptional regulator in photoconidiation. Expression analyses using microarrays containing 1438 unigenes were carried out in order to identify early light response genes. It was found that 2.8 % of the genes were light responsive: 2 % induced and 0.8 % repressed. Expression analysis in blr deletion mutants allowed the demonstration of the occurrence of two types of light responses, a blr-independent response in addition to the expected blr-dependent one, as well as a new role of the BLR proteins in repression of transcription. Exposure of T. atroviride to continuous light helped to establish that the light-responsive genes are subject to photoadaptation. Finally, evidence is provided of red-light-regulated gene expression and a possible crosstalk between the blue and red light signalling pathways.

[1]  K. Eichenberg,et al.  Rapid Blue Light Regulation of a Trichoderma harzianum Photolyase Gene* , 1999, The Journal of Biological Chemistry.

[2]  G. Macino,et al.  White collar 2, a partner in blue‐light signal transduction, controlling expression of light–regulated genes in Neurospora crassa , 1997, The EMBO journal.

[3]  R. Gomer,et al.  Overexpression of White Collar‐1 (WC‐1) activates circadian clock‐associated genes, but is not sufficient to induce most light‐regulated gene expression in Neurospora crassa , 2002, Molecular microbiology.

[4]  W. Cleveland,et al.  Locally Weighted Regression: An Approach to Regression Analysis by Local Fitting , 1988 .

[5]  J. Bok,et al.  LaeA, a Regulator of Secondary Metabolism in Aspergillus spp , 2004, Eukaryotic Cell.

[6]  Hongyu Zhao,et al.  Light Control of Arabidopsis Development Entails Coordinated Regulation of Genome Expression and Cellular Pathways , 2001, The Plant Cell Online.

[7]  G. Macino,et al.  The Neurospora crassa carotenoid biosynthetic gene (albino 3) reveals highly conserved regions among prenyltransferases. , 1991, The Journal of biological chemistry.

[8]  M. Schmoll,et al.  Envoy, a PAS/LOV Domain Protein of Hypocrea jecorina (Anamorph Trichoderma reesei), Modulates Cellulase Gene Transcription in Response to Light , 2005, Eukaryotic Cell.

[9]  R. Turner,et al.  Photoregulation of the Carotenoid Biosynthetic Pathway in Albino and White Collar Mutants of Neurospora crassa. , 1981, Plant physiology.

[10]  Yi Liu,et al.  Molecular mechanism of light responses in Neurospora: from light-induced transcription to photoadaptation. , 2005, Genes & development.

[11]  Michael Freitag,et al.  Lessons from the Genome Sequence of Neurospora crassa: Tracing the Path from Genomic Blueprint to Multicellular Organism , 2004, Microbiology and Molecular Biology Reviews.

[12]  R. Dean,et al.  An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. , 2003, Trends in biochemical sciences.

[13]  K. Folta,et al.  Opposing roles of phytochrome A and phytochrome B in early cryptochrome-mediated growth inhibition. , 2001, The Plant journal : for cell and molecular biology.

[14]  B. Horwitz,et al.  Characterization of Blue-light and Developmental Regulation of the Photolyase gene phr1 in Trichoderma harzianum , 2000, Photochemistry and photobiology.

[15]  J. Wessels,et al.  Hydrophobin Genes Involved in Formation of Aerial Hyphae and Fruit Bodies in Schizophyllum. , 1991, The Plant cell.

[16]  S. Dudoit,et al.  Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. , 2002, Nucleic acids research.

[17]  M. Gelb,et al.  Prenyl proteins in eukaryotic cells: a new type of membrane anchor. , 1990, Trends in biochemical sciences.

[18]  J. Christie,et al.  Phototropins 1 and 2: versatile plant blue-light receptors. , 2002, Trends in plant science.

[19]  M. Van Montagu,et al.  Trichoderma harzianum genes induced during growth on Rhizoctonia solani cell walls. , 1995, Microbiology.

[20]  C. Schwerdtfeger,et al.  VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation , 2003, The EMBO journal.

[21]  S. Shizukuishi,et al.  Purification and characterization from human parotid secretion of a peptide which inhibits hemagglutination of Bacteroides gingivalis 381. , 1990, FEMS microbiology letters.

[22]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[23]  D. Ebbole,et al.  rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa. , 1997, Genetics.

[24]  Light‐stimulated phosphorylation of proteins in cell‐free extracts from Trichoderma viride , 1989, FEBS letters.

[25]  V. Betina.  Photoinduced conidiation inTrichoderma viride , 1995, Folia Microbiologica (Prague).

[26]  J. Mullen,et al.  Phytochrome Modulation of Blue Light-Induced Chloroplast Movements in Arabidopsis1 , 2003, Plant Physiology.

[27]  J. Harborne.  Encyclopedia of plant physiology, New series , 1978 .

[28]  E. Oakeley,et al.  Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  V. Olmedo-Monfil,et al.  Cross Talk between a Fungal Blue-Light Perception System and the Cyclic AMP Signaling Pathway , 2006, Eukaryotic Cell.

[30]  G. Macino,et al.  Blue light regulation in Neurospora crassa. , 1997, Fungal genetics and biology : FG & B.

[31]  E. Galun.  Scanning Electron Microscopy of Intact Trichoderma Colonies , 1971, Journal of bacteriology.

[32]  B. Horwitz,et al.  Photoperception mutants in Trichoderma: mutants that sporulate in response to stress but not light , 1985, Current Genetics.

[33]  G. Macino,et al.  White collar‐1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. , 1996, The EMBO journal.

[34]  R. Vierstra,et al.  Genetic and Molecular Analysis of Phytochromes from the Filamentous Fungus Neurospora crassa , 2005, Eukaryotic Cell.

[35]  A. Herrera-Estrella,et al.  BLR-1 and BLR-2, key regulatory elements of photoconidiation and mycelial growth in Trichoderma atroviride. , 2004, Microbiology.

[36]  H. Inoue,et al.  The Neurospora uvs-2 gene encodes a protein which has homology to yeast RAD18, with unique zinc finger motifs , 1993, Molecular and General Genetics MGG.

[37]  T. Adams,et al.  Asexual Sporulation in Aspergillus nidulans , 1998, Microbiology and Molecular Biology Reviews.

[38]  J. Dunlap,et al.  White Collar-1, a Circadian Blue Light Photoreceptor, Binding to the frequency Promoter , 2002, Science.

[39]  C. Fankhauser,et al.  The Phytochromes, a Family of Red/Far-red Absorbing Photoreceptors* , 2001, The Journal of Biological Chemistry.

[40]  G. Macino,et al.  Protein kinase C modulates light responses in Neurospora by regulating the blue light photoreceptor WC‐1 , 2005, Molecular microbiology.

[41]  J. Haplová,et al.  Light-activated adenyl cyclase from Trichoderma viride. , 1992, FEMS microbiology letters.

[42]  R. Fischer,et al.  The Aspergillus nidulans Phytochrome FphA Represses Sexual Development in Red Light , 2005, Current Biology.

[43]  V. Monnier,et al.  The veA gene is necessary for the inducible expression by fructosyl amines of the Aspergillus nidulansfaoA gene encoding fructosyl amino acid oxidase (amadoriase, EC 1.5.3) , 2002, Archives of Microbiology.

[44]  E. Huala,et al.  Blue-light photoreceptors in higher plants. , 1999, Annual review of cell and developmental biology.

[45]  A. Herrera-Estrella,et al.  Trichoderma atroviride G-Protein α-Subunit Gene tga1 Is Involved in Mycoparasitic Coiling and Conidiation , 2002, Eukaryotic Cell.

[46]  V. Russo,et al.  Fast light-regulated genes of Neurospora crassa. , 1989, Nucleic acids research.

[47]  Z. Wang,et al.  A cis-acting region required for the regulated expression of grg-1, a Neurospora glucose-repressible gene. Two regulatory sites (CRE and NRS) are required to repress grg-1 expression. , 1994, Journal of molecular biology.

[48]  C. Schwerdtfeger,et al.  Localization and light-dependent phosphorylation of white collar 1 and 2, the two central components of blue light signaling in Neurospora crassa. , 2000, European journal of biochemistry.

[49]  K. Gardner,et al.  White Collar-1, a DNA Binding Transcription Factor and a Light Sensor , 2002, Science.

[50]  J. Lopes,et al.  Genetic regulation of phospholipid biosynthesis in Saccharomyces cerevisiae , 1996, Microbiological reviews.

[51]  H. Linden.  Blue Light Perception and Signal Transduction in Neurospora crassa , 2002 .

[52]  K. Langfelder,et al.  Biosynthesis of fungal melanins and their importance for human pathogenic fungi. , 2003, Fungal genetics and biology : FG & B.

[53]  A. Sancar,et al.  DNA repair enzymes. , 1988, Annual review of biochemistry.

[54]  N. Kolarova,et al.  Membrane potential, ATP, and cyclic AMP changes induced by light inTrichoderma viride , 1988 .

[55]  H. Mohr,et al.  Encyclopedia of plant physiology. New Series. Volume 16B. Photomorphogenesis. , 1983 .

[56]  V. Russo,et al.  Nitrogen regulation of blue light-inducible genes in Neurospora crassa , 1992 .