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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.

Show MeSH
Sizable proportions of poplar and rice transcriptomes display daily oscillations in RNA abundance with peak expression encompassing all phases of the day.Proportions of poplar and rice genes rhythmically (red sector) expressed under diurnal and free running (circadian) conditions. Transcripts were considered cyclically expressed if the Pearson correlation coefficient r between the data and respective HAYSTACK pattern model ([1], [11]; http://haystack.cgrb.oregonstate.edu/) was 0.75 or greater. The proportions were calculated as ratios of the number of the unique cycling genes to the total number of unique gene models represented on array. Diurnal and circadian segments of each time course were separated by a spacer period of forty eight hours of continuous light as described in the Materials and Methods.
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pone-0016907-g001: Sizable proportions of poplar and rice transcriptomes display daily oscillations in RNA abundance with peak expression encompassing all phases of the day.Proportions of poplar and rice genes rhythmically (red sector) expressed under diurnal and free running (circadian) conditions. Transcripts were considered cyclically expressed if the Pearson correlation coefficient r between the data and respective HAYSTACK pattern model ([1], [11]; http://haystack.cgrb.oregonstate.edu/) was 0.75 or greater. The proportions were calculated as ratios of the number of the unique cycling genes to the total number of unique gene models represented on array. Diurnal and circadian segments of each time course were separated by a spacer period of forty eight hours of continuous light as described in the Materials and Methods.

Mentions: Analyses of the resulting diurnal datasets showed that photocycles and thermocycles drove rhythmic expression of a sizable proportion of rice and poplar transcriptomes (Figure 1). The maximum number of rhythmic transcripts in both species was detected under driven (diurnal) conditions. All circadian (free running) conditions produced 2- to 4-fold fewer rhythmic transcripts than their respective diurnal conditions. In both rice and poplar the highest and the lowest proportions of the rhythmic transcripts under driven (diurnal) conditions were associated with photo- and thermocycles, respectively. The number of transcripts regulated by photo/thermocycles (LDHC) was intermediate as compared to photo- (LDHH) and thermocycles (LLHC) alone. Collectively, 60.9% (21,683 out of total 38,581 unique gene models) of P. trichocarpa and 59.5% (21,364 out of 35,928 unique gene models) of O. sativa ssp. japonica transcripts represented on arrays were expressed rhythmically under at least one diurnal condition (Figure 2). Using the phase calls provided by HAYSTACK algorithm we determined that rhythmic rice and poplar genes encompassed all phases of the day (Figure 3). Notably, a significant proportion of transcripts peaked a few hours before the light/dark transitions (dawn and dusk) resembling the bimodal distribution observed in Arabidopsis [1] and consistent with the expression of many circadian regulated genes in anticipation of the dawn and dusk light/dark transitions. The clusters of cycling genes with both high and low expression levels were evenly distributed across all phases of the day (Figure S7).


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)

Sizable proportions of poplar and rice transcriptomes display daily oscillations in RNA abundance with peak expression encompassing all phases of the day.Proportions of poplar and rice genes rhythmically (red sector) expressed under diurnal and free running (circadian) conditions. Transcripts were considered cyclically expressed if the Pearson correlation coefficient r between the data and respective HAYSTACK pattern model ([1], [11]; http://haystack.cgrb.oregonstate.edu/) was 0.75 or greater. The proportions were calculated as ratios of the number of the unique cycling genes to the total number of unique gene models represented on array. Diurnal and circadian segments of each time course were separated by a spacer period of forty eight hours of continuous light as described in the Materials and Methods.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3111414&req=5

pone-0016907-g001: Sizable proportions of poplar and rice transcriptomes display daily oscillations in RNA abundance with peak expression encompassing all phases of the day.Proportions of poplar and rice genes rhythmically (red sector) expressed under diurnal and free running (circadian) conditions. Transcripts were considered cyclically expressed if the Pearson correlation coefficient r between the data and respective HAYSTACK pattern model ([1], [11]; http://haystack.cgrb.oregonstate.edu/) was 0.75 or greater. The proportions were calculated as ratios of the number of the unique cycling genes to the total number of unique gene models represented on array. Diurnal and circadian segments of each time course were separated by a spacer period of forty eight hours of continuous light as described in the Materials and Methods.
Mentions: Analyses of the resulting diurnal datasets showed that photocycles and thermocycles drove rhythmic expression of a sizable proportion of rice and poplar transcriptomes (Figure 1). The maximum number of rhythmic transcripts in both species was detected under driven (diurnal) conditions. All circadian (free running) conditions produced 2- to 4-fold fewer rhythmic transcripts than their respective diurnal conditions. In both rice and poplar the highest and the lowest proportions of the rhythmic transcripts under driven (diurnal) conditions were associated with photo- and thermocycles, respectively. The number of transcripts regulated by photo/thermocycles (LDHC) was intermediate as compared to photo- (LDHH) and thermocycles (LLHC) alone. Collectively, 60.9% (21,683 out of total 38,581 unique gene models) of P. trichocarpa and 59.5% (21,364 out of 35,928 unique gene models) of O. sativa ssp. japonica transcripts represented on arrays were expressed rhythmically under at least one diurnal condition (Figure 2). Using the phase calls provided by HAYSTACK algorithm we determined that rhythmic rice and poplar genes encompassed all phases of the day (Figure 3). Notably, a significant proportion of transcripts peaked a few hours before the light/dark transitions (dawn and dusk) resembling the bimodal distribution observed in Arabidopsis [1] and consistent with the expression of many circadian regulated genes in anticipation of the dawn and dusk light/dark transitions. The clusters of cycling genes with both high and low expression levels were evenly distributed across all phases of the day (Figure S7).

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