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Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules.

Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, Michael TP, Chory J, Kay SA, Mockler TC - PLoS ONE (2011)

Bottom Line: The expression of many orthologous genes in key metabolic and regulatory pathways is diurnal and/or circadian regulated and phased to similar times of day.Our results confirm previous findings in Arabidopsis of three major classes of cis-regulatory modules within the plant circadian network: the morning (ME, GBOX), evening (EE, GATA), and midnight (PBX/TBX/SBX) modules.Identification of identical overrepresented motifs in the promoters of cycling genes from different species suggests that the core diurnal/circadian cis-regulatory network is deeply conserved between mono- and dicotyledonous species.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT

Background: Circadian clocks provide an adaptive advantage through anticipation of daily and seasonal environmental changes. In plants, the central clock oscillator is regulated by several interlocking feedback loops. It was shown that a substantial proportion of the Arabidopsis genome cycles with phases of peak expression covering the entire day. Synchronized transcriptome cycling is driven through an extensive network of diurnal and clock-regulated transcription factors and their target cis-regulatory elements. Study of the cycling transcriptome in other plant species could thus help elucidate the similarities and differences and identify hubs of regulation common to monocot and dicot plants.

Methodology/principal findings: Using a combination of oligonucleotide microarrays and data mining pipelines, we examined daily rhythms in gene expression in one monocotyledonous and one dicotyledonous plant, rice and poplar, respectively. Cycling transcriptomes were interrogated under different diurnal (driven) and circadian (free running) light and temperature conditions. Collectively, photocycles and thermocycles regulated about 60% of the expressed nuclear genes in rice and poplar. Depending on the condition tested, up to one third of oscillating Arabidopsis-poplar-rice orthologs were phased within three hours of each other suggesting a high degree of conservation in terms of rhythmic gene expression. We identified clusters of rhythmically co-expressed genes and searched their promoter sequences to identify phase-specific cis-elements, including elements that were conserved in the promoters of Arabidopsis, poplar, and rice.

Conclusions/significance: Our results show that the cycling patterns of many circadian clock genes are highly conserved across poplar, rice, and Arabidopsis. The expression of many orthologous genes in key metabolic and regulatory pathways is diurnal and/or circadian regulated and phased to similar times of day. Our results confirm previous findings in Arabidopsis of three major classes of cis-regulatory modules within the plant circadian network: the morning (ME, GBOX), evening (EE, GATA), and midnight (PBX/TBX/SBX) modules. Identification of identical overrepresented motifs in the promoters of cycling genes from different species suggests that the core diurnal/circadian cis-regulatory network is deeply conserved between mono- and dicotyledonous species.

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Identification of conserved cis-elements in promoters of Arabidopsis, rice and poplar genes cycling in the LDHH condition.ELEMENT-based enumerative promoter analysis and Z-score profile comparisons between rice, poplar and Arabidopsis. Z-score profiles were summarized for diurnal and circadian associated elements exhibiting conserved time-of-day overrepresentation across rice, poplar and Arabidopsis. A Z-score cutoff threshold value 2.33 corresponding to a p-value of 0.01 was selected arbitrarily. Time points 0 and 12 correspond to subjective dawn and dusk, respectively.
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pone-0016907-g010: Identification of conserved cis-elements in promoters of Arabidopsis, rice and poplar genes cycling in the LDHH condition.ELEMENT-based enumerative promoter analysis and Z-score profile comparisons between rice, poplar and Arabidopsis. Z-score profiles were summarized for diurnal and circadian associated elements exhibiting conserved time-of-day overrepresentation across rice, poplar and Arabidopsis. A Z-score cutoff threshold value 2.33 corresponding to a p-value of 0.01 was selected arbitrarily. Time points 0 and 12 correspond to subjective dawn and dusk, respectively.

Mentions: To identify cis-regulatory elements associated with diurnal/circadian regulation of rice and poplar gene expression, as well as motifs conserved with those in Arabidopsis [1], we mined the promoters of cycling poplar, rice, and Arabidopsis genes to identify DNA elements that could be associated with expression at a specific time of day. Using the HAYSTACK algorithm we identified clusters of co-expressed cycling genes in rice, poplar, and Arabidopsis. The putative promoters (500 base pairs upstream of the annotated gene model) for genes in each phase bin were searched for overrepresented 3–8-mer promoter elements (or words) using ELEMENT [1]. The resulting Z-scores were assembled into Z-score profiles corresponding to the 24 1-hour phases of the day and these Z-score profiles were further analyzed to identify profiles in which multiple consecutive Z-scores exceeded a threshold corresponding to a 5% false-discovery rate. The Z-score profiles were also compared between species using HAYSTACK to identify promoter elements with conserved enrichment profiles. This analysis revealed conserved diurnal- and circadian-associated promoter elements that were overrepresented among co-expressed genes in rice, poplar, and Arabidopsis at specific times of day (Figure 10). Motifs representing all phases of the day included the Morning Element (ME) [2], [18], Evening Element (EE) [2], GBOX [2], [19], [20], [21], GATA motif [22], [23], CBS [24], and SBX/TBX [1].


Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules.

Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, Michael TP, Chory J, Kay SA, Mockler TC - PLoS ONE (2011)

Identification of conserved cis-elements in promoters of Arabidopsis, rice and poplar genes cycling in the LDHH condition.ELEMENT-based enumerative promoter analysis and Z-score profile comparisons between rice, poplar and Arabidopsis. Z-score profiles were summarized for diurnal and circadian associated elements exhibiting conserved time-of-day overrepresentation across rice, poplar and Arabidopsis. A Z-score cutoff threshold value 2.33 corresponding to a p-value of 0.01 was selected arbitrarily. Time points 0 and 12 correspond to subjective dawn and dusk, respectively.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111414&req=5

pone-0016907-g010: Identification of conserved cis-elements in promoters of Arabidopsis, rice and poplar genes cycling in the LDHH condition.ELEMENT-based enumerative promoter analysis and Z-score profile comparisons between rice, poplar and Arabidopsis. Z-score profiles were summarized for diurnal and circadian associated elements exhibiting conserved time-of-day overrepresentation across rice, poplar and Arabidopsis. A Z-score cutoff threshold value 2.33 corresponding to a p-value of 0.01 was selected arbitrarily. Time points 0 and 12 correspond to subjective dawn and dusk, respectively.
Mentions: To identify cis-regulatory elements associated with diurnal/circadian regulation of rice and poplar gene expression, as well as motifs conserved with those in Arabidopsis [1], we mined the promoters of cycling poplar, rice, and Arabidopsis genes to identify DNA elements that could be associated with expression at a specific time of day. Using the HAYSTACK algorithm we identified clusters of co-expressed cycling genes in rice, poplar, and Arabidopsis. The putative promoters (500 base pairs upstream of the annotated gene model) for genes in each phase bin were searched for overrepresented 3–8-mer promoter elements (or words) using ELEMENT [1]. The resulting Z-scores were assembled into Z-score profiles corresponding to the 24 1-hour phases of the day and these Z-score profiles were further analyzed to identify profiles in which multiple consecutive Z-scores exceeded a threshold corresponding to a 5% false-discovery rate. The Z-score profiles were also compared between species using HAYSTACK to identify promoter elements with conserved enrichment profiles. This analysis revealed conserved diurnal- and circadian-associated promoter elements that were overrepresented among co-expressed genes in rice, poplar, and Arabidopsis at specific times of day (Figure 10). Motifs representing all phases of the day included the Morning Element (ME) [2], [18], Evening Element (EE) [2], GBOX [2], [19], [20], [21], GATA motif [22], [23], CBS [24], and SBX/TBX [1].

Bottom Line: The expression of many orthologous genes in key metabolic and regulatory pathways is diurnal and/or circadian regulated and phased to similar times of day.Our results confirm previous findings in Arabidopsis of three major classes of cis-regulatory modules within the plant circadian network: the morning (ME, GBOX), evening (EE, GATA), and midnight (PBX/TBX/SBX) modules.Identification of identical overrepresented motifs in the promoters of cycling genes from different species suggests that the core diurnal/circadian cis-regulatory network is deeply conserved between mono- and dicotyledonous species.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT

Background: Circadian clocks provide an adaptive advantage through anticipation of daily and seasonal environmental changes. In plants, the central clock oscillator is regulated by several interlocking feedback loops. It was shown that a substantial proportion of the Arabidopsis genome cycles with phases of peak expression covering the entire day. Synchronized transcriptome cycling is driven through an extensive network of diurnal and clock-regulated transcription factors and their target cis-regulatory elements. Study of the cycling transcriptome in other plant species could thus help elucidate the similarities and differences and identify hubs of regulation common to monocot and dicot plants.

Methodology/principal findings: Using a combination of oligonucleotide microarrays and data mining pipelines, we examined daily rhythms in gene expression in one monocotyledonous and one dicotyledonous plant, rice and poplar, respectively. Cycling transcriptomes were interrogated under different diurnal (driven) and circadian (free running) light and temperature conditions. Collectively, photocycles and thermocycles regulated about 60% of the expressed nuclear genes in rice and poplar. Depending on the condition tested, up to one third of oscillating Arabidopsis-poplar-rice orthologs were phased within three hours of each other suggesting a high degree of conservation in terms of rhythmic gene expression. We identified clusters of rhythmically co-expressed genes and searched their promoter sequences to identify phase-specific cis-elements, including elements that were conserved in the promoters of Arabidopsis, poplar, and rice.

Conclusions/significance: Our results show that the cycling patterns of many circadian clock genes are highly conserved across poplar, rice, and Arabidopsis. The expression of many orthologous genes in key metabolic and regulatory pathways is diurnal and/or circadian regulated and phased to similar times of day. Our results confirm previous findings in Arabidopsis of three major classes of cis-regulatory modules within the plant circadian network: the morning (ME, GBOX), evening (EE, GATA), and midnight (PBX/TBX/SBX) modules. Identification of identical overrepresented motifs in the promoters of cycling genes from different species suggests that the core diurnal/circadian cis-regulatory network is deeply conserved between mono- and dicotyledonous species.

Show MeSH
Related in: MedlinePlus