1 Instituto de Investigación en Biología Experimental, Facultad de Química, Universidad de Guanajuato, Apartado postal 187, Guanajuato 36050, Mexico
2 Departamento de Ingeniería Genética de Plantas, CINVESTAV Unidad Irapuato, Apartado postal 629, Irapuato 36500, Mexico
Correspondence
Alfredo Herrera-Estrella
aherrera{at}ira.cinvestav.mx
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the sequences reported in this paper are AY628431 for blr-1 and AY628432 for blr-2.
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INTRODUCTION |
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A second light response in T. atroviride is the regulation of the expression of the photolyase gene phr-1. Blue light and development regulate expression of phr-1. No phr-1 mRNA is detected in the dark, but it becomes detectable immediately after the light pulse (Berrocal-Tito et al., 1999). cAMP bypasses the requirement for light for sporulation, whereas atropine, a compound known to reduce cAMP levels in fungal cells, prevents sporulation even after photoinduction. Light regulation of phr1, however, is indifferent to both these effectors (Berrocal-Tito et al., 2000
). Induction of photolyase expression behaves as a direct, rapid response to light, independent of the induction of sporulation (Berrocal-Tito et al., 2000
). These data suggest either that photoconidiation and light-induced expression of phr-1 follow divergent signal transduction cascades or that conidiation is triggered indirectly by light, as a secondary response to the exposure to this stimulus.
The shape of the action spectrum of photoconidiation (Gressel & Hartmann, 1968; Kumagai & Oda, 1969
), which depicts the relative effectiveness of different wavelengths of light in eliciting the physiological response, is consistent with the absorption spectra of some flavoproteins. Experiments with the riboflavin structural analogue roseoflavin (Horwitz et al., 1984b
) also indicate the participation of a flavin as the photoreceptive pigment. Phototropism in higher plants (Thimann & Curry, 1960
), photocarotenogenesis in Neurospora crassa (De Fabo et al., 1976
), and many other biological responses to blue light, have similar action spectra (Senger, 1980
). Phototropism in higher plants is mediated by phototropins, serine-threonine protein kinases that undergo light-dependent autophosphorylation. The N-terminal region of these proteins contains two LOV (Light, Oxygen and Voltage) domains that bind FMN to function as light sensors (Christie et al., 1999
). The fluorescence excitation spectrum of the recombinant protein, and of isolated LOV domains, corresponds well with the action spectrum for phototropism (Christie et al., 1998
). All known responses to blue light in N. crassa are initiated by a pair of zinc finger transcription factors encoded by the white-collar genes (wc-1 and wc-2). Additionally, WC-1 and WC-2 are the positive components in a negative feedback loop central to the occurrence of circadian rhythms in Neurospora (Crosthwaite et al., 1997
). These rhythms are entrained by blue light and WC-1 is the photoreceptor controlling this response. WC-1 possesses a FAD-binding LOV domain that is very similar to those of phototropins and that also functions as a light sensor (Froehlich et al., 2002
; He et al., 2002
). WC-1 and WC-2 interact through PAS domains to form the functional white collar complex (WCC) that binds to the promoters of light-regulated genes to rapidly activate transcription in response to light (Talora et al., 1999
). Similarly, in T. atroviride phr-1 undergoes fast transcriptional activation in response to light (Berrocal-Tito et al., 1999
). The presence of putative WCC-binding boxes in the promoter region of phr-1 suggested that blue light responses in T. atroviride could be under the control of white collar homologues.
Here we demonstrate that disruption of the T. atroviride blr-1 and blr-2 genes, orthologues of wc-1 and wc-2, completely blocks photoconidiation and prevents the rapid blue-light-induced expression of phr-1. We also show for the first time the induction of a developmental process in an asexual fungus by injury, which is not altered in the blr mutants. Finally, we describe mycelial growth inhibition caused by both red and blue light, which is compensated by the presence of the BLR proteins.
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METHODS |
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Southern and Northern blot analysis.
Total RNA was extracted from mycelia as previously described (Berrocal-Tito et al., 2000) and used for Northern analysis following standard techniques (Sambrook & Russell, 2001
). For Northern blot analysis a 1·35 kb EcoRV fragment of phr-1 was labelled with 32P and used as a probe. A human 28S rDNA probe was used as loading control. DNA from each sample was isolated as described previously (Berrocal-Tito et al., 2000
). Southern blot analysis was performed following standard techniques (Sambrook & Russell, 2001
). A BamHI/PstI blr-1 fragment containing the complete gene and a HindIII blr-2 fragment containing the complete open reading frame were 32P labelled and used as probes for hybridization.
Isolation of blr-1 and blr-2.
The primers used for the amplification of the T. atroviride white-collar homologues were as follows. For the wc-1 homologue, the forward primer fwc1 (5'-GATTGTGCAAATTGCCATACGAGG-3') and reverse primer rwc1 (5'-CAACCCACAACTGTTGCATAGATC-3'), both identical to segments of the wc-1 gene, were used. For the wc-2 homologue, a set of degenerate primers was synthesized from reverse-translated segments of the WC-2 protein sequence, corresponding to the peptides EEYVCTDC for the forward primer (fwc2) and TLCNACGL for the reverse primer (rwc2). The resulting DNA fragments were labelled with a random-priming DNA-labelling system and used as probes to screen a EMBL3 genomic library of T. atroviride. For blr-1 the gene structure and coding sequence was predicted with the program GENSCAN (Burge & Karlin, 1997
). For blr-2 the coding sequence was determined by cDNA cloning and sequencing. Domain composition analyses for sequences were performed with Pfam (Bateman et al., 2002
) with an E value of 0·54; detecting the PAC motif in BLR-2 required lowering the sensitivity to E=8 (we define a PAS domain as the sum of Pfam-PAS and Pfam-PAC). The LOV domain alignments were performed with CLUSTAL X 1.83 (Thompson et al., 1997
).
Generation of blr mutants by gene replacement.
For the blr-1 subclone, a 1425 bp Eco47III fragment containing the three PAS domains was replaced by a 1·4 kbp HpaI fragment of the pCB1004 plasmid (Carroll et al., 1994). For the blr-2 subclone the entire coding sequence was removed by inserting an upstream BamHI/PstI fragment and a downstream XhoI fragment into the corresponding restriction sites of plasmid pBHY70, which contains the hygromycin B resistance cassette derived from plasmid pCB1004 in the EcoRV site. The constructs were used for transformation of T. atroviride. blr-1 mutants were obtained by biolistic transformation (Lorito et al., 1993
) and blr-2 mutants by PEG-mediated protoplast transformation as previously described (Baek & Kenerley, 1998
), except that mycelium was digested using 6 mg Novozyme ml1 (Novo Biolabs). For screening of the gene-replacement events, the DNA of hygromycin-resistant colonies was subjected to PCR using primers with sequences taken from genomic DNA next to blr-1 and blr-2 but not present in the constructs used to transform, together with a primer hybridizing to the hph gene. Positive colonies were made to sporulate by injury, as described below, and serial dilutions of spore suspensions were plated to obtain monosporic cultures for three cycles.
RT-PCR.
Total RNA of wild-type, blr-1 and
blr-2 strains was obtained and incubated with DNase (Invitrogen) at 37 °C for 1 h. Two 5 µg samples of RNA of each mutant strain and four 5 µg samples of the wild-type strain were taken for standard RT reactions, except for controls without reverse transcriptase. For PCR amplification of the blr-1 transcript cDNA, the forward primer BLR606 (5'-GGGATGACAGCCGAAC-3') and the reverse primer BLR569 (5'-TCAGCTCCCGCGTGAC-3') were used, spanning 1277 bp. Primer BLR569 corresponds to a sequence found in the second PAS domain of the protein that was deleted in the mutant and BLR606 to a sequence found in the 5' translated portion of the gene that remained intact. For PCR amplification of the blr-2 transcript cDNA, the forward primer 2316 (5'-CATTGCGGCTGCTAGG-3') and the reverse primer 2180 (5'-GTCCCTTTCGCCATTC-3') were used, spanning 629 bp. In this case both primers were designed within the deleted region of the gene. For the amplification of the slt-2 transcript cDNA, the forward primer AHE-G300 (5'-AGACGCATCGTGCCA-3') and the reverse primer 1738 (5'-TCGGCCTTGCTCGTGG-3') were used, spanning 450 bp.
Light-effect experiments.
Colonies were induced to conidiate as previously described (Berrocal-Tito et al., 1999), by exposure to a standard blue light source consisting of light from cool-white fluorescent tubes filtered through a blue acrylic filter (LEE no. 183; fluence rate 3 µmol m2 s1). For RNA extractions the colonies were inoculated over a washed cellophane sheet overlaying the solid media. At various times, the mycelia were scraped from the surface of the cellophane under red safelight (0·1 µmol m2 s1). Samples of mycelia exposed to light or kept in the dark were immediately frozen in liquid nitrogen and used for RNA extraction. For colony growth inhibition experiments the same cool-white fluorescent tubes were used, without filter for white light (fluence rate 13 µmol m2 s1), with the LEE no. 183 filter for blue light (fluence rate 4·3 µmol m2 s1) and with a LEE no. 182 filter for red light (fluence rate 3·1 µmol m2 s1); all incubations were done at 25 °C.
Stress-induced conidiation assays.
For injury-induced conidiation, fungal colonies were grown in total darkness on PDA at 25 °C for 72 h, cut in stripes with a scalpel and incubated for an additional 24 h in the dark at 25 °C.
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RESULTS |
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DISCUSSION |
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Northern blots carried out to detect the mRNA of both blr-1 and blr-2 showed that they are transcriptionally active and that the corresponding transcripts do not appear to be significantly affected by light (data not shown). As expected, T. atroviride mutants in either blr-1 or blr-2, where the gene was replaced by a deleted version, were shown (by RT-PCR, Fig. 3) to lack the corresponding transcript. These mutants were unable to conidiate in response to blue light and no induction of the light-responsive gene phr-1 could be observed. An interesting observation showing that the conidiation process is not affected in the BLR mutants is the response to injury. The induction by injury of a developmental process in fungi was described in Schizophyllum commune for haploid fruiting-body formation (Leonard & Dick, 1973
). However, to the best of our knowledge, induction of asexual reproduction by injury has not been previously reported in filamentous fungi.
As mentioned before, PAS domains are implicated in signal transduction in a wide variety of organisms and also in the formation of proteinprotein interactions, as between WC-1 and WC-2 (Cheng et al., 2002). By analogy to what occurs in Neurospora, the BLR proteins may function as a complex to activate transcription of fast light-regulated genes such as phr-1. The DNA-binding domains and the nuclear localization signal in BLR-1, the presence in the phr-1 promoter of elements similar to those necessary for the WC complex binding to the promoter of Neurospora genes, the similar time-course of fast light-regulated genes in both organisms, and the fact that the induction of phr-1 mRNA is abolished in the blr mutants, argue in favour of this possibility. However, a third protein carrying typical activation domains could be necessary to form an active complex if the glutamine-rich region in the N-terminus of BLR-1 is not functional.
T. atroviride was chosen as a photobiological model due to the apparent simplicity of its single known response to light. Here we describe another response that must depend on other blue and/or red light receptor(s). The growth rate of the wild-type and blr mutant strains is reduced in constant white light relative to dark-grown colonies. The effect of light on growth rate is exacerbated when the colonies are grown in constant blue or red light, suggesting that a balance is attained when both types of light are given in conjunction (white light). Mycelial growth inhibition by blue but not red light has recently been described in the hypogeous fungus Tuber borchii. The authors describe a similar effect of blue light in N. crassa, and suggest that this response in N. crassa depends on the presence of a functional WC-1 protein (Ambra et al., 2004). In contrast, in Trichoderma the exacerbated mycelial growth inhibition by exposure to constant blue light can only be observed in the absence of either blr-1 or blr-2. The presence of the BLR proteins in the wild-type strain seems to protect against the exacerbated effect of constant blue but not red light. This apparent contradiction can be explained by the fact that in T. atroviride all strains, mutant and wild-type, grow faster in the dark than when exposed to white light and that the blr mutants have a higher growth rate, both in the dark and when exposed to light, than the wild-type (see Fig. 6a
). In fact, after careful examination of the data reported for N. crassa a similar behaviour can be observed; we believe that this phenomenon is what is actually described by Ambra et al. (2004)
, where if only growth under illumination is considered the phenomenon seems to be white-collar 1 dependent. Further support for our interpretation comes from the fact that the data presented by Ambra et al. (2004)
also show a marked growth inhibition by white light in the wc-1 mutant, similar to the effect observed in the T. atroviride blr-1 mutant when using this type of light. Unfortunately, no data are available on the effect of different types of light on mycelial growth inhibition in Neurospora and Tuber borchii does not appear to respond to red light. Additionally, the conditions to which both fungi were exposed are not comparable and we know of no further photobiological work on the effect of different light intensities in T. borchii. Taken together, our data suggest that mycelial growth inhibition at least in T. atroviride is mediated by an as-yet-unidentified blue-light receptor. The effect of red light was surprising because these wavelengths were previously thought to have no effect in Trichoderma.
A possible explanation for these phenomena is that normal mycelial growth of the T. atroviride blr mutants when exposed to constant white light can only be achieved if there is an interaction between the two putative blue and red light receptors or their corresponding signalling pathways. Crosstalk between blue and red light signalling pathways is well documented in plants (Nagy & Schafer, 2002). This would imply that the separate effects of blue and red light are not additive when the fungus is exposed to both types of light but rather that the interaction blocks both detrimental effects as a result of signal integration. An alternative explanation is that yet another receptor perceiving light outside of the blue and red regions of the spectrum, perhaps green light, compensates for the negative effect of blue and red light. Recently, a green-light-absorbing rhodopsin was reported in N. crassa (Brown et al., 2001
). There is increasing evidence of green light antagonizing the effects of blue and red light in plants, such as stomatal opening and stem elongation (Folta, 2004
; Talbott et al., 2002
). Normal growth under constant blue light would necessarily require the interaction between the BLR photoreceptor system and that of the novel blue light receptor proposed. This would imply that the BLR proteins are involved in sustaining mycelial growth when mycelium is exposed to constant blue light and it is not competent for sporulation. It is possible that photoreceptor(s), similar to cry-1, vvd, phy-1 or phy-2, recently found in the N. crassa genome (Borkovich et al., 2004
) play a role in the control of mycelial growth.
Blue light is a potent stimulus with the potential to induce harmful photosensitized reactions inside cells; most organisms compensate for this in ways that are not always obvious. Fungi are no exception: N. crassa responds by synthesizing screening pigments and the soil fungus T. atroviride sporulates. The effect of light on growth rate shown here resembles that of stressful conditions such as nutrient limitation and high temperature. It is thus possible that the BLR proteins have a more general role in dealing with stress. The absence of end of plate conidiation and the faster growth of the mutants point to light-independent functions of these proteins. One such function could be participation in a probable circadian rhythm observed in Trichoderma; an approximately 24 h oscillation of light sensitivity for the photoinduced conidiation was reported (Deitzer et al., 1988), and a light pulse results in a shift of the banding pattern of a mutant that sporulates in the dark (Deitzer et al., 1984
). BLAST searches against several newly sequenced fungal genomes revealed proteins similar to BLR-1 and BLR-2 in several of them, such as Fusarium graminearum, Podospora anserina, Nectria haematococca, Magnaporthe grisea, Aspergillus nidulans and Ustilago maydis. Thus it appears that BLR-like proteins are conserved fungal regulators possibly involved in coping with blue-light-induced stress and other stressing stimuli, although until now the function of proteins belonging to this family had only been shown for the N. crassa WC-1 and WC-2.
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ACKNOWLEDGEMENTS |
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Received 20 May 2004;
revised 12 July 2004;
accepted 12 August 2004.
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