Temperate woody plants have developed sophisticated winter survival and maintenance mechanisms that enable them to adapt rapidly to the annual cycle of environmental changes. Here, we demonstrate notable aspects of the transcriptional regulation adopted by poplar in winter/dormancy, employing biochemical and whole transcriptome analysis, and showing high levels of transcriptional activity in a broad spectrum of genes during the dormancy period. A total of 3237 probe sets upregulated more than threefold in winter/dormancy stems over summer/active-growth stems were identified. As expected, genes related to cold hardiness and defense were over-represented. Carbohydrate biosynthesis and transport-related genes were also actively expressed in winter/dormancy stems. Further biochemical analyses verified the dormancy/winter transcription phenotype. More than 60% of the winter upregulated transcription factors (TFs) were related to either biotic or abiotic stress. This finding substantiates that the major transcriptional network of winter/dormancy stems is related to stress tolerance, such as dehydration, cold tolerance and defense. Furthermore, during winter/dormancy, preferential expression of genes involved in cell wall biosynthesis or modification, indirect transcriptional regulation (RNA metabolism) and chromatin modification/remodeling were observed. Taken together, these findings show that regulation of gene expression associated with winter survival and maintenance extends beyond control by promoter-binding TFs to include regulation at the post-transcriptional and chromatin levels.

Heartwood is a determining factor of wood quality and understanding the biology of heartwood may allow us to control its formation. Heartwood formation is a form of senescence that is accompanied by a variety of metabolic alterations in ray parenchyma cells at the sapwood-heartwood transition zone. Although senescence has been studied at the molecular level with respect to primary growth, the cell maturation and death events occurring during heartwood formation have been difficult to study because of their location and timing. Analysis of global gene expression patterns during the transition from sapwood to heartwood may offer a powerful means of identifying the mechanisms controlling heartwood formation. Previously, we developed cDNA microarrays carrying 2567 unigenes derived from the bark/cambium region, sapwood and transition zone of a mature black locust tree. Here, we describe the use of these microarrays to characterize seasonal changes in the expression patterns of 1873 genes from the transition zone of mature black locust trees. When samples collected in summer and fall were compared, 569 genes showed differential expression patterns: 293 genes were up-regulated (> twofold) in summer (July 5) and 276 genes were up-regulated in fall (November 27). More than 50% of the secondary and hormone metabolism-related genes on the microarrays were up-regulated in summer. Twenty-nine out of 55 genes involved in signal transduction were differentially regulated, suggesting that the ray parenchyma cells located in the innermost part of the trunk wood react to seasonal changes. We established the expression patterns of 349 novel genes (previously unknown or no-hit), of which 154 were up-regulated in summer and 195 were up-regulated in the fall.

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.

Cycling between vegetative growth and dormancy is an important adaptive mechanism in temperate woody plants. To gain insights into the underlying molecular mechanisms, we carried out global transcription analyses on stem samples from poplar (Populus deltoides Bartr. ex Marsh.) trees grown in the field and in controlled environments. Among seasonal changes in the transcriptome, up-regulation of defense-related genes predominated in early winter, whereas signaling-related genes were up-regulated during late winter. Cluster analysis of the differentially expressed genes showed that plants regulated seasonal growth by integrating environmental factors with development. Short day lengths induced some cold-associated genes without concomitant low temperature exposure, and enhanced the expression of some genes when combined with low temperature exposure. These mechanisms appear to maintain closer synchrony between cold hardiness and climate than would be achieved through responses to temperature alone.