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Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis.

Jin H, Vacic V, Girke T, Lonardi S, Zhu JK - BMC Mol. Biol. (2008)

Bottom Line: However, the extent of siRNA-mediated regulation of cis-NAT genes is still unclear in any genome.The hallmarks of RNAi regulation of NATs are 1) inverse regulation of two genes in a cis-NAT pair by environmental and developmental cues and 2) generation of siRNAs by cis-NAT genes.By searching the Arabidopsis Small RNA Project (ASRP) and Massively Parallel Signature Sequencing (MPSS) small RNA databases as well as our stress-treated small RNA dataset, we found small RNAs that matched at least one gene in 646 pairs out of 1008 (64%) protein-coding cis-NAT pairs, which suggests that siRNAs may regulate the expression of many cis-NAT genes. 209 putative siRNAs have the potential to target more than one gene and half of these small RNAs could target multiple members of a gene family.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Plant Pathology, Center for Plant Cell Biology and Institute for Integrative Genome Biology, University of California, Riverside, CA 92521, USA. hailingj@ucr.edu

ABSTRACT

Background: In spite of large intergenic spaces in plant and animal genomes, 7% to 30% of genes in the genomes encode overlapping cis-natural antisense transcripts (cis-NATs). The widespread occurrence of cis-NATs suggests an evolutionary advantage for this type of genomic arrangement. Experimental evidence for the regulation of two cis-NAT gene pairs by natural antisense transcripts-generated small interfering RNAs (nat-siRNAs) via the RNA interference (RNAi) pathway has been reported in Arabidopsis. However, the extent of siRNA-mediated regulation of cis-NAT genes is still unclear in any genome.

Results: The hallmarks of RNAi regulation of NATs are 1) inverse regulation of two genes in a cis-NAT pair by environmental and developmental cues and 2) generation of siRNAs by cis-NAT genes. We examined Arabidopsis transcript profiling data from public microarray databases to identify cis-NAT pairs whose sense and antisense transcripts show opposite expression changes. A subset of the cis-NAT genes displayed negatively correlated expression profiles as well as inverse differential expression changes under at least one of the examined developmental stages or treatment conditions. By searching the Arabidopsis Small RNA Project (ASRP) and Massively Parallel Signature Sequencing (MPSS) small RNA databases as well as our stress-treated small RNA dataset, we found small RNAs that matched at least one gene in 646 pairs out of 1008 (64%) protein-coding cis-NAT pairs, which suggests that siRNAs may regulate the expression of many cis-NAT genes. 209 putative siRNAs have the potential to target more than one gene and half of these small RNAs could target multiple members of a gene family. Furthermore, the majority of the putative siRNAs within the overlapping regions tend to target only one transcript of a given NAT pair, which is consistent with our previous finding on salt- and bacteria-induced nat-siRNAs. In addition, we found that genes encoding plastid- or mitochondrion-targeted proteins are over-represented in the Arabidopsis cis-NATs and that 19% of sense and antisense partner genes of cis-NATs share at least one common Gene Ontology term, which suggests that they encode proteins with possible functional connection.

Conclusion: The negatively correlated expression patterns of sense and antisense genes as well as the presence of siRNAs in many of the cis-NATs suggest that siRNA regulation of cis-NATs via the RNAi pathway is an important gene regulatory mechanism for at least a subgroup of cis-NATs in Arabidopsis.

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Pearson correlation coefficients for the cis-NAT pairs and non-overlapping gene pairs plotted to form a density plot. The corresponding means, standard deviations and p-values are in Table 2.
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Figure 2: Pearson correlation coefficients for the cis-NAT pairs and non-overlapping gene pairs plotted to form a density plot. The corresponding means, standard deviations and p-values are in Table 2.

Mentions: Figure 2 shows that the distribution of the correlation coefficients of the cis-NAT dataset is slightly shifted toward lower coefficients as compared with the corresponding data set for all non-overlapping gene pairs in the Arabidopsis genome. The very low p-value of a two-sample t-test (Table 2) indicates that this difference is statistically significant, whereas the difference for randomized gene pairs (500 iterations) is less pronounced. We also observed slight positive correlations between neighboring genes, which may be explained by common chromatin configurations, transcriptional hot spots or other factors.


Small RNAs and the regulation of cis-natural antisense transcripts in Arabidopsis.

Jin H, Vacic V, Girke T, Lonardi S, Zhu JK - BMC Mol. Biol. (2008)

Pearson correlation coefficients for the cis-NAT pairs and non-overlapping gene pairs plotted to form a density plot. The corresponding means, standard deviations and p-values are in Table 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2262095&req=5

Figure 2: Pearson correlation coefficients for the cis-NAT pairs and non-overlapping gene pairs plotted to form a density plot. The corresponding means, standard deviations and p-values are in Table 2.
Mentions: Figure 2 shows that the distribution of the correlation coefficients of the cis-NAT dataset is slightly shifted toward lower coefficients as compared with the corresponding data set for all non-overlapping gene pairs in the Arabidopsis genome. The very low p-value of a two-sample t-test (Table 2) indicates that this difference is statistically significant, whereas the difference for randomized gene pairs (500 iterations) is less pronounced. We also observed slight positive correlations between neighboring genes, which may be explained by common chromatin configurations, transcriptional hot spots or other factors.

Bottom Line: However, the extent of siRNA-mediated regulation of cis-NAT genes is still unclear in any genome.The hallmarks of RNAi regulation of NATs are 1) inverse regulation of two genes in a cis-NAT pair by environmental and developmental cues and 2) generation of siRNAs by cis-NAT genes.By searching the Arabidopsis Small RNA Project (ASRP) and Massively Parallel Signature Sequencing (MPSS) small RNA databases as well as our stress-treated small RNA dataset, we found small RNAs that matched at least one gene in 646 pairs out of 1008 (64%) protein-coding cis-NAT pairs, which suggests that siRNAs may regulate the expression of many cis-NAT genes. 209 putative siRNAs have the potential to target more than one gene and half of these small RNAs could target multiple members of a gene family.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Plant Pathology, Center for Plant Cell Biology and Institute for Integrative Genome Biology, University of California, Riverside, CA 92521, USA. hailingj@ucr.edu

ABSTRACT

Background: In spite of large intergenic spaces in plant and animal genomes, 7% to 30% of genes in the genomes encode overlapping cis-natural antisense transcripts (cis-NATs). The widespread occurrence of cis-NATs suggests an evolutionary advantage for this type of genomic arrangement. Experimental evidence for the regulation of two cis-NAT gene pairs by natural antisense transcripts-generated small interfering RNAs (nat-siRNAs) via the RNA interference (RNAi) pathway has been reported in Arabidopsis. However, the extent of siRNA-mediated regulation of cis-NAT genes is still unclear in any genome.

Results: The hallmarks of RNAi regulation of NATs are 1) inverse regulation of two genes in a cis-NAT pair by environmental and developmental cues and 2) generation of siRNAs by cis-NAT genes. We examined Arabidopsis transcript profiling data from public microarray databases to identify cis-NAT pairs whose sense and antisense transcripts show opposite expression changes. A subset of the cis-NAT genes displayed negatively correlated expression profiles as well as inverse differential expression changes under at least one of the examined developmental stages or treatment conditions. By searching the Arabidopsis Small RNA Project (ASRP) and Massively Parallel Signature Sequencing (MPSS) small RNA databases as well as our stress-treated small RNA dataset, we found small RNAs that matched at least one gene in 646 pairs out of 1008 (64%) protein-coding cis-NAT pairs, which suggests that siRNAs may regulate the expression of many cis-NAT genes. 209 putative siRNAs have the potential to target more than one gene and half of these small RNAs could target multiple members of a gene family. Furthermore, the majority of the putative siRNAs within the overlapping regions tend to target only one transcript of a given NAT pair, which is consistent with our previous finding on salt- and bacteria-induced nat-siRNAs. In addition, we found that genes encoding plastid- or mitochondrion-targeted proteins are over-represented in the Arabidopsis cis-NATs and that 19% of sense and antisense partner genes of cis-NATs share at least one common Gene Ontology term, which suggests that they encode proteins with possible functional connection.

Conclusion: The negatively correlated expression patterns of sense and antisense genes as well as the presence of siRNAs in many of the cis-NATs suggest that siRNA regulation of cis-NATs via the RNAi pathway is an important gene regulatory mechanism for at least a subgroup of cis-NATs in Arabidopsis.

Show MeSH
Related in: MedlinePlus