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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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Gene ontology (GO) categories overrepresented among rice (ssp. japonica) cycling genes under photoperiods (LDHH).The shaded circles indicate overrepresented GO categories (categories with FDR≤0.05 are shown in yellow) based on significance level. The radius of each circle denotes the number of genes in each category. The list of cycling genes was generated using HAYSTACK with best fitting model cutoff value r≥0.9. GO overrepresentation graph was generated using the network visualization tool Cytoscape (http://www.cytoscape.org/).
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pone-0016907-g008: Gene ontology (GO) categories overrepresented among rice (ssp. japonica) cycling genes under photoperiods (LDHH).The shaded circles indicate overrepresented GO categories (categories with FDR≤0.05 are shown in yellow) based on significance level. The radius of each circle denotes the number of genes in each category. The list of cycling genes was generated using HAYSTACK with best fitting model cutoff value r≥0.9. GO overrepresentation graph was generated using the network visualization tool Cytoscape (http://www.cytoscape.org/).

Mentions: The analysis of gene ontology (GO) categories associated with cycling genes revealed several GO terms overrepresented among oscillating rice (ssp. japonica) genes. Thus, under photocycles (LDHH) rice cycling genes were associated with GO categories such as lipid and carbohydrate metabolic processes, photosynthesis, nucleotide binding, translation, and amino acid and nucleotide metabolism (Figure 8). Under photocycles, these and several other overrepresented GO categories overlapped between rice and poplar (Figure S3). Mapping of oscillating genes to the 339 currently defined metabolic pathways in the RiceCyc database (http://www.gramene.org/pathway/, [15]) suggested that many of the major metabolic pathways in rice are under diurnal and/or circadian control. Under photocycles, a total of 2,078 rhythmically expressed genes mapped to defined metabolic pathways of rice (Figure S4). We found multiple examples of metabolic pathways that were broadly represented at every step by cycling genes, although secondary metabolic pathways showed the least representation by cycling genes (Figure S5).


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)

Gene ontology (GO) categories overrepresented among rice (ssp. japonica) cycling genes under photoperiods (LDHH).The shaded circles indicate overrepresented GO categories (categories with FDR≤0.05 are shown in yellow) based on significance level. The radius of each circle denotes the number of genes in each category. The list of cycling genes was generated using HAYSTACK with best fitting model cutoff value r≥0.9. GO overrepresentation graph was generated using the network visualization tool Cytoscape (http://www.cytoscape.org/).
© Copyright Policy
Related In: Results  -  Collection

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

pone-0016907-g008: Gene ontology (GO) categories overrepresented among rice (ssp. japonica) cycling genes under photoperiods (LDHH).The shaded circles indicate overrepresented GO categories (categories with FDR≤0.05 are shown in yellow) based on significance level. The radius of each circle denotes the number of genes in each category. The list of cycling genes was generated using HAYSTACK with best fitting model cutoff value r≥0.9. GO overrepresentation graph was generated using the network visualization tool Cytoscape (http://www.cytoscape.org/).
Mentions: The analysis of gene ontology (GO) categories associated with cycling genes revealed several GO terms overrepresented among oscillating rice (ssp. japonica) genes. Thus, under photocycles (LDHH) rice cycling genes were associated with GO categories such as lipid and carbohydrate metabolic processes, photosynthesis, nucleotide binding, translation, and amino acid and nucleotide metabolism (Figure 8). Under photocycles, these and several other overrepresented GO categories overlapped between rice and poplar (Figure S3). Mapping of oscillating genes to the 339 currently defined metabolic pathways in the RiceCyc database (http://www.gramene.org/pathway/, [15]) suggested that many of the major metabolic pathways in rice are under diurnal and/or circadian control. Under photocycles, a total of 2,078 rhythmically expressed genes mapped to defined metabolic pathways of rice (Figure S4). We found multiple examples of metabolic pathways that were broadly represented at every step by cycling genes, although secondary metabolic pathways showed the least representation by cycling genes (Figure S5).

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