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Upstream regulatory architecture of rice genes: summarizing the baseline towards genus-wide comparative analysis of regulatory networks and allele mining.

de Los Reyes BG, Mohanty B, Yun SJ, Park MR, Lee DY - Rice (N Y) (2015)

Bottom Line: Such information is also important to establish the foundation for mining non-coding sequence variation that defines novel alleles and epialleles across the enormous phenotypic diversity represented in rice germplasm.This review presents a synthesis of the state of knowledge and consensus trends regarding the various cis-acting and trans-acting components that define spatio-temporal regulation of rice genes based on representative examples from both foundational studies in other model and non-model plants, and more recent studies in rice.Perspectives on the potential applications of such information for gene discovery, network engineering and genomics-enabled rice breeding are also discussed.

View Article: PubMed Central - PubMed

Affiliation: School of Biology and Ecology, University of Maine, Orono, ME 04469 USA.

ABSTRACT
Dissecting the upstream regulatory architecture of rice genes and their cognate regulator proteins is at the core of network biology and its applications to comparative functional genomics. With the rapidly advancing comparative genomics resources in the genus Oryza, a reference genome annotation that defines the various cis-elements and trans-acting factors that interface each gene locus with various intrinsic and extrinsic signals for growth, development, reproduction and adaptation must be established to facilitate the understanding of phenotypic variation in the context of regulatory networks. Such information is also important to establish the foundation for mining non-coding sequence variation that defines novel alleles and epialleles across the enormous phenotypic diversity represented in rice germplasm. This review presents a synthesis of the state of knowledge and consensus trends regarding the various cis-acting and trans-acting components that define spatio-temporal regulation of rice genes based on representative examples from both foundational studies in other model and non-model plants, and more recent studies in rice. The goal is to summarize the baseline for systematic upstream sequence annotation of the rapidly advancing genome sequence resources in Oryza in preparation for genus-wide functional genomics. Perspectives on the potential applications of such information for gene discovery, network engineering and genomics-enabled rice breeding are also discussed.

No MeSH data available.


Related in: MedlinePlus

Hypothetical and simplistic models of upstream regulatory information content of spatio-temporally regulated genes of rice.(A) Prototype inducible promoter is comprised of combinations of cis-elements (i.e., colored boxes upstream from the core promoter identified by lowercase letters) that directly interface gene induction/represssion with various environmental and developmental signals. This occurs by virtue of their respective cognate regulatory transcription factors (i.e., TF1, TF2, etc.) that respond to hormonal or other physico-chemical changes in the cell. The spatio-temporal properties of genes are therefore defined by the integration of external and developmental cues through the synergistic interactions of various cis-elements and their cognate regulatory transcription factors. (B) Example of a pattern/trend that could be revealed by phylogenetic footprinting of upstream regulatory sequences of rice genes with potential significance to comparative functional genomics and allele mining. Phylogenetic footprinting has suggested that functional differences between the promoters of genes that vary in spatio-temporal regulation may be due to combinations of divergent regulatory fine-tuner elements (colored squares) and highly conserved core module elements (black squares). Variation in cis-regulatory information content may therefore reveal the genomic basis for variant alleles with unique spatio-temporal properties. This concept may be extrapolated for interspecific comparisons of orthologs and paralogs towards the discovery of potential novel alleles in the genus Oryza. Differences in expression in the absence of apparent upstream sequence variation may be used as basis for targeted analysis of differential methylation (shown with asterisks*) of homologous promoters. This concept may have potential applications for the discovery of epialleles that determine phenotypic variation.
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Fig3: Hypothetical and simplistic models of upstream regulatory information content of spatio-temporally regulated genes of rice.(A) Prototype inducible promoter is comprised of combinations of cis-elements (i.e., colored boxes upstream from the core promoter identified by lowercase letters) that directly interface gene induction/represssion with various environmental and developmental signals. This occurs by virtue of their respective cognate regulatory transcription factors (i.e., TF1, TF2, etc.) that respond to hormonal or other physico-chemical changes in the cell. The spatio-temporal properties of genes are therefore defined by the integration of external and developmental cues through the synergistic interactions of various cis-elements and their cognate regulatory transcription factors. (B) Example of a pattern/trend that could be revealed by phylogenetic footprinting of upstream regulatory sequences of rice genes with potential significance to comparative functional genomics and allele mining. Phylogenetic footprinting has suggested that functional differences between the promoters of genes that vary in spatio-temporal regulation may be due to combinations of divergent regulatory fine-tuner elements (colored squares) and highly conserved core module elements (black squares). Variation in cis-regulatory information content may therefore reveal the genomic basis for variant alleles with unique spatio-temporal properties. This concept may be extrapolated for interspecific comparisons of orthologs and paralogs towards the discovery of potential novel alleles in the genus Oryza. Differences in expression in the absence of apparent upstream sequence variation may be used as basis for targeted analysis of differential methylation (shown with asterisks*) of homologous promoters. This concept may have potential applications for the discovery of epialleles that determine phenotypic variation.

Mentions: Creating novel combinations of superior alleles by integrative use of conventional and biotechnological methods is the overarching goal of 21st century rice breeding. The genome-enabled research paradigm in rice biology has contributed to this goal through the understanding of gene function and regulation. Moreover, at the very core of the reference genome-guided research paradigm is the quest to pinpoint useful allelic variation in the germplasm that explains simple or quantitative traits to guide targeted introgression and selection. Broadly, gene function can be described in the context of a gene’s specific molecular, biochemical and/or biological roles in the cell and in context of its role in a broader molecular or biochemical network. The upstream regulatory sequence signature of a gene is a window to the combinatorial complexity of its regulation and reflects how it is interfaced with the various intrinsic and extrinsic signals for growth, development, reproduction and adaptation (Figure 3A). In these contexts, a truly biologically meaningful annotation of the reference genomes of rice that could facilitate a holistic understanding of the nature of allelic and epiallelic variation for phenotypes of interest must include information on the critical cis-elements and trans-acting factors that define the spatio-temporal regulatory properties of each gene. Establishing a modular map of regulatory elements within the upstream regions of each gene locus as part of reference genome annotations in a similar manner that we understand protein domain architectures of coding sequences will be an important tool for various applications in comparative functional genomics both at the intraspecific and interspecific levels.Figure 3


Upstream regulatory architecture of rice genes: summarizing the baseline towards genus-wide comparative analysis of regulatory networks and allele mining.

de Los Reyes BG, Mohanty B, Yun SJ, Park MR, Lee DY - Rice (N Y) (2015)

Hypothetical and simplistic models of upstream regulatory information content of spatio-temporally regulated genes of rice.(A) Prototype inducible promoter is comprised of combinations of cis-elements (i.e., colored boxes upstream from the core promoter identified by lowercase letters) that directly interface gene induction/represssion with various environmental and developmental signals. This occurs by virtue of their respective cognate regulatory transcription factors (i.e., TF1, TF2, etc.) that respond to hormonal or other physico-chemical changes in the cell. The spatio-temporal properties of genes are therefore defined by the integration of external and developmental cues through the synergistic interactions of various cis-elements and their cognate regulatory transcription factors. (B) Example of a pattern/trend that could be revealed by phylogenetic footprinting of upstream regulatory sequences of rice genes with potential significance to comparative functional genomics and allele mining. Phylogenetic footprinting has suggested that functional differences between the promoters of genes that vary in spatio-temporal regulation may be due to combinations of divergent regulatory fine-tuner elements (colored squares) and highly conserved core module elements (black squares). Variation in cis-regulatory information content may therefore reveal the genomic basis for variant alleles with unique spatio-temporal properties. This concept may be extrapolated for interspecific comparisons of orthologs and paralogs towards the discovery of potential novel alleles in the genus Oryza. Differences in expression in the absence of apparent upstream sequence variation may be used as basis for targeted analysis of differential methylation (shown with asterisks*) of homologous promoters. This concept may have potential applications for the discovery of epialleles that determine phenotypic variation.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4385054&req=5

Fig3: Hypothetical and simplistic models of upstream regulatory information content of spatio-temporally regulated genes of rice.(A) Prototype inducible promoter is comprised of combinations of cis-elements (i.e., colored boxes upstream from the core promoter identified by lowercase letters) that directly interface gene induction/represssion with various environmental and developmental signals. This occurs by virtue of their respective cognate regulatory transcription factors (i.e., TF1, TF2, etc.) that respond to hormonal or other physico-chemical changes in the cell. The spatio-temporal properties of genes are therefore defined by the integration of external and developmental cues through the synergistic interactions of various cis-elements and their cognate regulatory transcription factors. (B) Example of a pattern/trend that could be revealed by phylogenetic footprinting of upstream regulatory sequences of rice genes with potential significance to comparative functional genomics and allele mining. Phylogenetic footprinting has suggested that functional differences between the promoters of genes that vary in spatio-temporal regulation may be due to combinations of divergent regulatory fine-tuner elements (colored squares) and highly conserved core module elements (black squares). Variation in cis-regulatory information content may therefore reveal the genomic basis for variant alleles with unique spatio-temporal properties. This concept may be extrapolated for interspecific comparisons of orthologs and paralogs towards the discovery of potential novel alleles in the genus Oryza. Differences in expression in the absence of apparent upstream sequence variation may be used as basis for targeted analysis of differential methylation (shown with asterisks*) of homologous promoters. This concept may have potential applications for the discovery of epialleles that determine phenotypic variation.
Mentions: Creating novel combinations of superior alleles by integrative use of conventional and biotechnological methods is the overarching goal of 21st century rice breeding. The genome-enabled research paradigm in rice biology has contributed to this goal through the understanding of gene function and regulation. Moreover, at the very core of the reference genome-guided research paradigm is the quest to pinpoint useful allelic variation in the germplasm that explains simple or quantitative traits to guide targeted introgression and selection. Broadly, gene function can be described in the context of a gene’s specific molecular, biochemical and/or biological roles in the cell and in context of its role in a broader molecular or biochemical network. The upstream regulatory sequence signature of a gene is a window to the combinatorial complexity of its regulation and reflects how it is interfaced with the various intrinsic and extrinsic signals for growth, development, reproduction and adaptation (Figure 3A). In these contexts, a truly biologically meaningful annotation of the reference genomes of rice that could facilitate a holistic understanding of the nature of allelic and epiallelic variation for phenotypes of interest must include information on the critical cis-elements and trans-acting factors that define the spatio-temporal regulatory properties of each gene. Establishing a modular map of regulatory elements within the upstream regions of each gene locus as part of reference genome annotations in a similar manner that we understand protein domain architectures of coding sequences will be an important tool for various applications in comparative functional genomics both at the intraspecific and interspecific levels.Figure 3

Bottom Line: Such information is also important to establish the foundation for mining non-coding sequence variation that defines novel alleles and epialleles across the enormous phenotypic diversity represented in rice germplasm.This review presents a synthesis of the state of knowledge and consensus trends regarding the various cis-acting and trans-acting components that define spatio-temporal regulation of rice genes based on representative examples from both foundational studies in other model and non-model plants, and more recent studies in rice.Perspectives on the potential applications of such information for gene discovery, network engineering and genomics-enabled rice breeding are also discussed.

View Article: PubMed Central - PubMed

Affiliation: School of Biology and Ecology, University of Maine, Orono, ME 04469 USA.

ABSTRACT
Dissecting the upstream regulatory architecture of rice genes and their cognate regulator proteins is at the core of network biology and its applications to comparative functional genomics. With the rapidly advancing comparative genomics resources in the genus Oryza, a reference genome annotation that defines the various cis-elements and trans-acting factors that interface each gene locus with various intrinsic and extrinsic signals for growth, development, reproduction and adaptation must be established to facilitate the understanding of phenotypic variation in the context of regulatory networks. Such information is also important to establish the foundation for mining non-coding sequence variation that defines novel alleles and epialleles across the enormous phenotypic diversity represented in rice germplasm. This review presents a synthesis of the state of knowledge and consensus trends regarding the various cis-acting and trans-acting components that define spatio-temporal regulation of rice genes based on representative examples from both foundational studies in other model and non-model plants, and more recent studies in rice. The goal is to summarize the baseline for systematic upstream sequence annotation of the rapidly advancing genome sequence resources in Oryza in preparation for genus-wide functional genomics. Perspectives on the potential applications of such information for gene discovery, network engineering and genomics-enabled rice breeding are also discussed.

No MeSH data available.


Related in: MedlinePlus