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. 2006 Dec 25:7:323.
doi: 10.1186/1471-2164-7-323.

Conservation of noncoding microsatellites in plants: implication for gene regulation

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Conservation of noncoding microsatellites in plants: implication for gene regulation

Lida Zhang et al. BMC Genomics. .

Abstract

Background: Microsatellites are extremely common in plant genomes, and in particular, they are significantly enriched in the 5' noncoding regions. Although some 5' noncoding microsatellites involved in gene regulation have been described, the general properties of microsatellites as regulatory elements are still unknown. To address the question of microsatellites associated with regulatory elements, we have analyzed the conserved noncoding microsatellite sequences (CNMSs) in the 5' noncoding regions by inter- and intragenomic phylogenetic footprinting in the Arabidopsis and Brassica genomes.

Results: We identified 247 Arabidopsis-Brassica orthologous and 122 Arabidopsis paralogous CNMSs, representing 491 CT/GA and CTT/GAA repeats, which accounted for 10.6% of these types located in the 500-bp regions upstream of coding sequences in the Arabidopsis genome. Among these identified CNMSs, 18 microsatellites show high conservation in the regulatory regions of both orthologous and paralogous genes, and some of them also appear in the corresponding positions of more distant homologs in Arabidopsis, as well as in other plants. A computational scan of CNMSs for known cis-regulatory elements showed that light responsive elements were clustered in the region of CT/GA repeats, as well as salicylic acid responsive elements in the (CTT)n/(GAA)n sequences. Patterns of gene expression revealed that 70-80% of CNMS (CTT)n/(GAA)n associated genes were regulated by salicylic acid, which was consistent with the prediction of regulatory elements in silico.

Conclusion: Our analyses showed that some noncoding microsatellites were conserved in plants and appeared to be ancient. These CNMSs served as regulatory elements involved in light and salicylic acid responses. Our findings might have implications in the common features of the over-represented microsatellites for gene regulation in plant-specific pathways.

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Figures

Figure 1
Figure 1
Distribution of microsatellites in different genomic regions in Arabidopsis. (A) Frequencies of dinucleotide repeats in different genomic fractions. Other dimers include all dimers except CT/GA repeats. (B) Frequencies of trinucleotide repeats in different genomic fractions. Other triplets include all triplets except CTT/GAA repeats. 5'-flanks correspond to the 500 bp sequences upstream of the initiation codon.
Figure 2
Figure 2
Distribution of (A) orthologous and (B) paralogous CNMSs in the 5' noncoding regions in Arabidopsis. The position is indicated as segments of 100 bp.
Figure 3
Figure 3
Occurrences of CNMSs in the random datasets. Dataset 1, dataset 2 and dataset 3 respectively correspond to the 1000 homologous pairs, the 1000 shuffled pairs of noncoding sequences and the 1000 random pairs of genomic sequences in the analysis. Sequence length is 500 bp. Occurrences of CNMSs were analyzed in analogous manner for 10 different random sets with equal data size. Means of CNMS occurrences are indicated on the y axis, and error bars represent SEs.
Figure 4
Figure 4
Distribution of synonymous substitution rate (Ks) for CNMS gene sets. (A) Distribution of Ks values for Arabidopsis-Brassica orthologous CNMS gene set. A clear peak for Ks values of 0.4 to 0.5. (B) Distribution of Ks values for paralogous CNMS gene set in Arabidopsis. Two clear peak for the Ks values of 0.8 to 0.9 and 1.2 to 1.3.
Figure 5
Figure 5
An example of microsatellites conserved among paralogous and orthologous genes. Sequence alignments and positions for the microsatellites conserved among (A) Arabidopsis paralogous genes, (B) Arabidopsis-Brassica orthologous genes and (C) homologous genes from Arabidopsis and Brassica. Boxed regions indicate CNMSs. Dots indicate omits of alignment. Nucleotide positions are given relative to the initiation codon.
Figure 6
Figure 6
Conservation of microsatellites in plants. (A) Sequence alignments for the CNMS conserved among the homologous protein kinase genes from Arabidopsis, Brassica, Medicago and rice. Atlg07870, At2g28590, BONGE63TR, BONRT22TR, AC135230_13 and Os07g49470 are orthologs for the four species. Sequences of Medicago (AC135230_13) and rice (Os07g49470) obtained from TIGR plant genome sequence database. (B) Sequence alignments for the CNMS conserved among the homologous GATA transcription factor genes from Arabidopsis, Brassica and rice. BONAX55TR and At2g45050 are orthologs for Brassica and Arabidopsis. The homologous gene Os05g44400 from rice.
Figure 7
Figure 7
Annotation enrichment and depletion of CNMS associated genes. In the top half of the figure, the maroon bars ("observed") give the numbers of orthologous CNMS genes that are annotated in the Arabidopsis GO database with molecular function "transcription factor activity" or biological process "transcription regulation" and "DNA metabolism". The blue bars ("expected") give the number of genes that one would expect to obtain if the same number of genes were chosen at random among all genes annotated in the relevant database. The bottom half of the figure gives similar information for paralogous CNMS genes in Arabidopsis.
Figure 8
Figure 8
Expression patterns of (A) orthologous and (B) paralogous CNMS (CTT)n/(GAA)n associated genes in Arabidopsis leaves with salicylic acid treatment. Genes were inhibited after 4 hours of treatment with salicylic acid (green), induced after 4 hours of treatment with salicylic acid (red) and kept inactive until 52 hours of treatment with salicylic acid (black). The gene expression levels were estimated by Arabidopsis MPSS data from three different libraries generated by untreated leaves and treated leaves 4 (S04) and 52 hours (S52) after salicylic acid treatment, respectively. TPM is normalized value in transcripts per million for each signature in the library.
Figure 9
Figure 9
Expression patterns of Arabidopsis CNMS (CTT)n/(GAA)n associated genes and their related sequence information. The expression of genes were assayed by RT-PCR. Lanes 1–5: control (untreated), 1, 4, 12 and 48 hours after treatment with 1 mM salicylic acid, respectively. The actin2 gene was used as an internal control in the RT-PCR reaction.

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