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A molecular framework for seasonal growth-dormancy regulation in perennial plants.

Shim D, Ko JH, Kim WC, Wang Q, Keathley DE, Han KH - Hortic Res (2014)

Bottom Line: Analyses of transcriptome changes during dormancy transitions have identified MADS-box transcription factors associated with endodormancy induction.A growing body of knowledge also indicates epigenetic regulation plays a role in these processes in perennial horticultural and forestry plants.The increased knowledge contributes to better understanding of the dormancy process and consequently to precise manipulation of dormancy-related horticultural traits, such as flowering time.

View Article: PubMed Central - PubMed

Affiliation: Schatz Center for Tree Molecular Genetics, Pennsylvania State University , University Park, PA16802, USA.

ABSTRACT
The timing of the onset and release of dormancy impacts the survival, productivity and spatial distribution of temperate horticultural and forestry perennials and is mediated by at least three main regulatory programs involving signal perception and processing by phytochromes (PHYs) and PHY-interacting transcription factors (PIFs). PIF4 functions as a key regulator of plant growth in response to both external and internal signals. In poplar, the expression of PIF4 and PIF3-LIKE1 is upregulated in response to short days, while PHYA and PHYB are not regulated at the transcriptional level. Integration of light and environmental signals is achieved by gating the expression and transcriptional activity of PIF4. During this annual cycle, auxin promotes the degradation of Aux/IAA transcriptional repressors through the SKP-Cullin-F-boxTIR1 complex, relieving the repression of auxin-responsive genes by allowing auxin response factors (ARFs) to activate the transcription of auxin-responsive genes involved in growth responses. Analyses of transcriptome changes during dormancy transitions have identified MADS-box transcription factors associated with endodormancy induction. Previous studies show that poplar dormancy-associated MADS-box (DAM) genes PtMADS7 and PtMADS21 are differentially regulated during the growth-dormancy cycle. Endodormancy may be regulated by internal factors, which are specifically localized in buds. PtMADS7/PtMADS21 may function as an internal regulator in poplar. The control of flowering time shares certain regulatory hierarchies with control of the dormancy/growth cycle. However, the particularities of different stages of the dormancy/growth cycle warrant comprehensive approaches to identify the causative genes for the entire cycle. A growing body of knowledge also indicates epigenetic regulation plays a role in these processes in perennial horticultural and forestry plants. The increased knowledge contributes to better understanding of the dormancy process and consequently to precise manipulation of dormancy-related horticultural traits, such as flowering time.

No MeSH data available.


Related in: MedlinePlus

Heat map of 52 genes that are associated with epigenetic regulation during the dormancy cycle. To show their normalized expression levels according to eight different growth-dormancy cycle stages, we used our unpublished RNA-Seq data to create a heat map for the genes involved in DNA methylation, histone modification, chromatin remodeling and polycomb group (PcG). The gene expression values were normalized by RPKM method. Red and green in the heat map mean upregulated and downregulated genes, respectively. Growth-dormancy cycle stages are active growth (AG), stop growth (SG), start of endodormancy (SEn), endodormancy (En), start of ecodormancy (SEc), transition of ecodormancy (Tr), ecodormancy (Ec) and growth resumption (EG).
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fig2: Heat map of 52 genes that are associated with epigenetic regulation during the dormancy cycle. To show their normalized expression levels according to eight different growth-dormancy cycle stages, we used our unpublished RNA-Seq data to create a heat map for the genes involved in DNA methylation, histone modification, chromatin remodeling and polycomb group (PcG). The gene expression values were normalized by RPKM method. Red and green in the heat map mean upregulated and downregulated genes, respectively. Growth-dormancy cycle stages are active growth (AG), stop growth (SG), start of endodormancy (SEn), endodormancy (En), start of ecodormancy (SEc), transition of ecodormancy (Tr), ecodormancy (Ec) and growth resumption (EG).

Mentions: There is growing evidence that genome-wide epigenetic regulation of gene expression is involved in dormancy regulation (for reviews) (Table 1).90,91 Whole-genome DNA methylation and acetylated histone 4 (H4) analyses in chestnut (Castanea sativa) showed higher DNA methylation ratios and lower H4 acetylation levels in dormant buds compared to actively growing tissues,92,93 suggesting gene silencing concomitant with bud dormancy. In hybrid aspen, putative histone deacetylases (HDA14 and HDA08), histone lysine methyltranferase (SUVR3) and histone ubiquitination involved gene (HUB2) were upregulated during growth-dormancy transition, while several Trithorax family genes counteracting the repressive effect of Polycomb complex and putative DEMETER-like DNA glycosylases are downregulated.89 These results suggest that some unknown active growth regulating genes might be repressed during dormancy induction through chromatin compaction mechanisms, such as histone deacetylation and methylation, histone ubiquitination, DNA methylation and Polycomb activity. Ko et al.14 also reported that many genes involved in chromatin remodeling/modification in poplar (e.g., including BRAT1, SWI2/SNF2, NFC2 and PAF1) showed upregulation in winter/dormancy stems, suggesting the dynamic nature of winter/dormancy-responsive gene regulation at chromatin level (Figure 2).


A molecular framework for seasonal growth-dormancy regulation in perennial plants.

Shim D, Ko JH, Kim WC, Wang Q, Keathley DE, Han KH - Hortic Res (2014)

Heat map of 52 genes that are associated with epigenetic regulation during the dormancy cycle. To show their normalized expression levels according to eight different growth-dormancy cycle stages, we used our unpublished RNA-Seq data to create a heat map for the genes involved in DNA methylation, histone modification, chromatin remodeling and polycomb group (PcG). The gene expression values were normalized by RPKM method. Red and green in the heat map mean upregulated and downregulated genes, respectively. Growth-dormancy cycle stages are active growth (AG), stop growth (SG), start of endodormancy (SEn), endodormancy (En), start of ecodormancy (SEc), transition of ecodormancy (Tr), ecodormancy (Ec) and growth resumption (EG).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4591672&req=5

fig2: Heat map of 52 genes that are associated with epigenetic regulation during the dormancy cycle. To show their normalized expression levels according to eight different growth-dormancy cycle stages, we used our unpublished RNA-Seq data to create a heat map for the genes involved in DNA methylation, histone modification, chromatin remodeling and polycomb group (PcG). The gene expression values were normalized by RPKM method. Red and green in the heat map mean upregulated and downregulated genes, respectively. Growth-dormancy cycle stages are active growth (AG), stop growth (SG), start of endodormancy (SEn), endodormancy (En), start of ecodormancy (SEc), transition of ecodormancy (Tr), ecodormancy (Ec) and growth resumption (EG).
Mentions: There is growing evidence that genome-wide epigenetic regulation of gene expression is involved in dormancy regulation (for reviews) (Table 1).90,91 Whole-genome DNA methylation and acetylated histone 4 (H4) analyses in chestnut (Castanea sativa) showed higher DNA methylation ratios and lower H4 acetylation levels in dormant buds compared to actively growing tissues,92,93 suggesting gene silencing concomitant with bud dormancy. In hybrid aspen, putative histone deacetylases (HDA14 and HDA08), histone lysine methyltranferase (SUVR3) and histone ubiquitination involved gene (HUB2) were upregulated during growth-dormancy transition, while several Trithorax family genes counteracting the repressive effect of Polycomb complex and putative DEMETER-like DNA glycosylases are downregulated.89 These results suggest that some unknown active growth regulating genes might be repressed during dormancy induction through chromatin compaction mechanisms, such as histone deacetylation and methylation, histone ubiquitination, DNA methylation and Polycomb activity. Ko et al.14 also reported that many genes involved in chromatin remodeling/modification in poplar (e.g., including BRAT1, SWI2/SNF2, NFC2 and PAF1) showed upregulation in winter/dormancy stems, suggesting the dynamic nature of winter/dormancy-responsive gene regulation at chromatin level (Figure 2).

Bottom Line: Analyses of transcriptome changes during dormancy transitions have identified MADS-box transcription factors associated with endodormancy induction.A growing body of knowledge also indicates epigenetic regulation plays a role in these processes in perennial horticultural and forestry plants.The increased knowledge contributes to better understanding of the dormancy process and consequently to precise manipulation of dormancy-related horticultural traits, such as flowering time.

View Article: PubMed Central - PubMed

Affiliation: Schatz Center for Tree Molecular Genetics, Pennsylvania State University , University Park, PA16802, USA.

ABSTRACT
The timing of the onset and release of dormancy impacts the survival, productivity and spatial distribution of temperate horticultural and forestry perennials and is mediated by at least three main regulatory programs involving signal perception and processing by phytochromes (PHYs) and PHY-interacting transcription factors (PIFs). PIF4 functions as a key regulator of plant growth in response to both external and internal signals. In poplar, the expression of PIF4 and PIF3-LIKE1 is upregulated in response to short days, while PHYA and PHYB are not regulated at the transcriptional level. Integration of light and environmental signals is achieved by gating the expression and transcriptional activity of PIF4. During this annual cycle, auxin promotes the degradation of Aux/IAA transcriptional repressors through the SKP-Cullin-F-boxTIR1 complex, relieving the repression of auxin-responsive genes by allowing auxin response factors (ARFs) to activate the transcription of auxin-responsive genes involved in growth responses. Analyses of transcriptome changes during dormancy transitions have identified MADS-box transcription factors associated with endodormancy induction. Previous studies show that poplar dormancy-associated MADS-box (DAM) genes PtMADS7 and PtMADS21 are differentially regulated during the growth-dormancy cycle. Endodormancy may be regulated by internal factors, which are specifically localized in buds. PtMADS7/PtMADS21 may function as an internal regulator in poplar. The control of flowering time shares certain regulatory hierarchies with control of the dormancy/growth cycle. However, the particularities of different stages of the dormancy/growth cycle warrant comprehensive approaches to identify the causative genes for the entire cycle. A growing body of knowledge also indicates epigenetic regulation plays a role in these processes in perennial horticultural and forestry plants. The increased knowledge contributes to better understanding of the dormancy process and consequently to precise manipulation of dormancy-related horticultural traits, such as flowering time.

No MeSH data available.


Related in: MedlinePlus