Limits...
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

Related in: MedlinePlus

Rhythmic expression of poplar and rice transcription factor transcripts.A. A large portion of the P. trichocarpa and O. sativa TFs represented on arrays are rhythmically expressed under photo-, thermo-, and photo/thermocycles. B. Rhythmically expressed TF transcripts encompass all phases of the day peaking a few hours before light/dark transitions. Poplar and rice TFs cycling in driven condition are listed in Table S1. B. Peak expression of cycling TFs occurs at all phases of the day. Expression heat maps of Populus trichocarpa and O. sativa (ssp. japonica) TFs oscillating under photocyles (LDHH). Mean centered expression levels are depicted in yellow (high expression) and blue (low expression). The heat map was generated using HAYSTACK output filtered using a Pearson correlation coefficient cutoff value r≥0.9.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3111414&req=5

pone-0016907-g009: Rhythmic expression of poplar and rice transcription factor transcripts.A. A large portion of the P. trichocarpa and O. sativa TFs represented on arrays are rhythmically expressed under photo-, thermo-, and photo/thermocycles. B. Rhythmically expressed TF transcripts encompass all phases of the day peaking a few hours before light/dark transitions. Poplar and rice TFs cycling in driven condition are listed in Table S1. B. Peak expression of cycling TFs occurs at all phases of the day. Expression heat maps of Populus trichocarpa and O. sativa (ssp. japonica) TFs oscillating under photocyles (LDHH). Mean centered expression levels are depicted in yellow (high expression) and blue (low expression). The heat map was generated using HAYSTACK output filtered using a Pearson correlation coefficient cutoff value r≥0.9.

Mentions: We further investigated rhythmic expression of transcription factors (TFs). For Populus trichocarpa, 2,052 (out of total predicted 2,576) TF genes (http://dptf.cbi.pku.edu.cn/, [16]) were represented on the Affymetrix poplar array. The O. sativa (ssp. japonica) microarrays represented 2,134 out of 2,384 predicted japonica rice TFs (http://drtf.cbi.pku.edu.cn/, [17]). Among those, 64.2% (1,318 non-redundant P. trichocarpa gene models) and 61.2% (1,307 non-redundant O. sativa, ssp. japonica gene models) of putative TF transcripts detectable on the microarrays cycled under at least one diurnal condition in poplar and rice, respectively. The proportions and partitioning of oscillating TFs among the different timecourse conditions was broadly consistent with the distributions among all cycling genes, i.e., the highest number of rhythmically expressed was driven by photocycles, the lowest – by thermocycles (Figure 9A). Several hundred genes encoding TFs displayed oscillating expression patterns under all tested diurnal conditions. Similar to the bulk of all nuclear-encoded genes, the expression profiles of cycling rice and poplar TFs showed a bimodal frequency distribution peaking at dusk and dawn (Figure 9B).


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)

Rhythmic expression of poplar and rice transcription factor transcripts.A. A large portion of the P. trichocarpa and O. sativa TFs represented on arrays are rhythmically expressed under photo-, thermo-, and photo/thermocycles. B. Rhythmically expressed TF transcripts encompass all phases of the day peaking a few hours before light/dark transitions. Poplar and rice TFs cycling in driven condition are listed in Table S1. B. Peak expression of cycling TFs occurs at all phases of the day. Expression heat maps of Populus trichocarpa and O. sativa (ssp. japonica) TFs oscillating under photocyles (LDHH). Mean centered expression levels are depicted in yellow (high expression) and blue (low expression). The heat map was generated using HAYSTACK output filtered using a Pearson correlation coefficient cutoff value r≥0.9.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0016907-g009: Rhythmic expression of poplar and rice transcription factor transcripts.A. A large portion of the P. trichocarpa and O. sativa TFs represented on arrays are rhythmically expressed under photo-, thermo-, and photo/thermocycles. B. Rhythmically expressed TF transcripts encompass all phases of the day peaking a few hours before light/dark transitions. Poplar and rice TFs cycling in driven condition are listed in Table S1. B. Peak expression of cycling TFs occurs at all phases of the day. Expression heat maps of Populus trichocarpa and O. sativa (ssp. japonica) TFs oscillating under photocyles (LDHH). Mean centered expression levels are depicted in yellow (high expression) and blue (low expression). The heat map was generated using HAYSTACK output filtered using a Pearson correlation coefficient cutoff value r≥0.9.
Mentions: We further investigated rhythmic expression of transcription factors (TFs). For Populus trichocarpa, 2,052 (out of total predicted 2,576) TF genes (http://dptf.cbi.pku.edu.cn/, [16]) were represented on the Affymetrix poplar array. The O. sativa (ssp. japonica) microarrays represented 2,134 out of 2,384 predicted japonica rice TFs (http://drtf.cbi.pku.edu.cn/, [17]). Among those, 64.2% (1,318 non-redundant P. trichocarpa gene models) and 61.2% (1,307 non-redundant O. sativa, ssp. japonica gene models) of putative TF transcripts detectable on the microarrays cycled under at least one diurnal condition in poplar and rice, respectively. The proportions and partitioning of oscillating TFs among the different timecourse conditions was broadly consistent with the distributions among all cycling genes, i.e., the highest number of rhythmically expressed was driven by photocycles, the lowest – by thermocycles (Figure 9A). Several hundred genes encoding TFs displayed oscillating expression patterns under all tested diurnal conditions. Similar to the bulk of all nuclear-encoded genes, the expression profiles of cycling rice and poplar TFs showed a bimodal frequency distribution peaking at dusk and dawn (Figure 9B).

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