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. 2003 Dec;133(4):1605-16.
doi: 10.1104/pp.103.030437.

Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data

Matthew E Hudson  1 , Peter H Quail
Affiliations

Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data

Matthew E Hudson et al. Plant Physiol. 2003 Dec.

Abstract

Several hundred Arabidopsis genes, transcriptionally regulated by phytochrome A (phyA), were previously identified using an oligonucleotide microarray. We have now identified, in silico, conserved sequence motifs in the promoters of these genes by comparing the promoter sequences to those of all the genes present on the microarray from which they were sampled. This was done using a Perl script (called Sift) that identifies over-represented motifs using an enumerative approach. The utility of Sift was verified by analysis of circadian-regulated promoters known to contain a biologically significant motif. Several elements were then identified in phyA-responsive promoters by their over-representation. Five previously undescribed motifs were detected in the promoters of phyA-induced genes. Four novel motifs were found in phyA-repressed promoters, plus a motif that strongly resembles the DE1 element. The G-box, CACGTG, was a prominent hit in both induced and repressed phyA-responsive promoters. Intriguingly, two distinct flanking consensus sequences were observed adjacent to the G-box core sequence: one predominating in phyA-induced promoters, the other in phyA-repressed promoters. Such different conserved flanking nucleotides around the core motif in these two sets of promoters may indicate that different members of the same family of DNA-binding proteins mediate phyA induction and repression. An increased abundance of G-box sequences was observed in the most rapidly phyA-responsive genes and in the promoters of phyA-regulated transcription factors, indicating that G-box-binding transcription factors are upstream components in a transcriptional cascade that mediates phyA-regulated development.

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Figures

Figure 1.
Figure 1.
Elements over-represented in circadian-regulated promoters. These are elements found in the promoters of circadian-regulated genes identified by Harmer et al. (2000). Each sequence shown was individually identified as a statistically significant over-represented sequence in circadian gene promoters. The sequences in each aligned group are those we determined to represent the same motif. The P value was determined using the binomial distribution to find the likelihood of the observed number of elements occurring in a randomly chosen set of promoters. The letters bs or ss designate whether the element was detected as over-represented on both strands (bs) or just one strand (ss).
Figure 2.
Figure 2.
Elements over-represented in phyA-induced promoters. These are elements found in the promoters of phytochrome-A-induced genes identified by Tepperman et al. (2001). Each sequence shown was individually identified as a statistically significant over-represented sequence in phyA-induced gene promoters. The sequences in each aligned group are those we determined to represent the same motif. The P value was determined using the binomial distribution to find the likelihood of the observed number of elements occurring in a randomly chosen set of promoters. The letters bs or ss designate whether the element was detected as over-represented on both strands (bs) or just one strand (ss).
Figure 3.
Figure 3.
Elements over-represented in phyA-repressed promoters. These are elements found in the promoters of phytochrome-A-repressed genes identified by Tepperman et al. (2001). Each sequence shown was individually identified as a statistically significant over-represented sequence in light-repressed gene promoters. The sequences in each aligned group are those we determined to represent the same motif. The P value was determined using the binomial distribution to find the likelihood of the observed number of elements occurring in a randomly chosen set of promoters. The letters bs or ss designate whether the element was detected as over-represented on both strands (bs) or just one strand (ss).
Figure 4.
Figure 4.
Distribution of motifs by promoter response. The graph shows the percentage of promoters containing putative and known light-regulatory sequence motifs. The promoters are grouped by their response to far-red light (early, transcripts that respond 2-fold within 1 h; late, transcripts that respond 2-fold within 24 h; up or down indicate the direction of the response to the stimulus). The bars show the percentage of promoters in each list containing an exact sequence match to the sequence given by the vertical axis.
Figure 5.
Figure 5.
Distribution of motifs by functional class of the downstream gene. The graphs each show the percentage of phyA-regulated genes in a given functional category containing an exact sequence motif in the promoter. The genes are grouped by the far-red-light response (induced [up] or repressed [down]) and by the functional category of the gene product. Functional categories are: PC, photosynthesis and chloroplast; CM, cellular metabolism related; GD, growth and development; HR, hormone related; TP, transmembrane transporters; TN, transcription; SD, stress and defense; SI, signaling; HY, hypothetical or unknown function (categories as defined by Tepperman et al. [2001]).
Figure 6.
Figure 6.
Distinct conserved flanking nucleotides of the G-boxes in phyA-induced and -repressed promoters may indicate a branch point in a transcriptional cascade. G-boxes are common in the promoters of the “first wave” of phyA-responsive genes. The active form of phyA is known to bind to bHLH proteins, which then bind G-box sequences. Genes encoding transcriptional regulators are prominent among these early-responding genes. The G-box/bHLH system is therefore correlated with both rapid induction and rapid repression of transcriptional regulators, making it the first step in a transcriptional cascade. Induction or repression is specified according to the flanking nucleotides around the CACGTG core. The consensus sequence of the G-boxes in phyA-induced promoters is CCACGTGTCA. The repressed promoters may be bound by yet to be discovered bHLH repressor proteins, specific to the conserved nucleotides CCACGTGAAG. The downstream events from the rapidly phyA-repressed transcriptional regulators remain to be characterized.
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