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Plant Signal Behav. 2009 October; 4(10): 959–961.
PMCID: PMC2801361

Regulation of cell cycle regulators by environmental signals during growth-dormancy cycle of trees

Abstract

Climate change such as changing temperature and increasing concentrations of atmospheric CO2, are likely to drive significant modifications in forests. While many studies have demonstrated the responses and adoptions of tree to fluctuations in climatic and environmental conditions, the impact of environmental signals on trees is complex and poorly understood with respect to the molecular biology in context of the seasonal change of environmental signals. This addendum is focused on the impact of environmental signals on growth-dormancy cycle of trees growing in temperate regions, especially the regulation of cell cycle regulators by temperature and photoperiod. In addition, the plant hormone control of growth-dormancy cycle of trees and cell cycle regulators in the cambium is also discussed.

Key words: cell cycle regulators, environmental signals, growth-dormancy cycle of trees, temperature

Growth-dormancy cycle of trees growing in temperate zones is driven by environmental cues, such as photoperiod and temperature, and it involves regular division of meristem cells in shoot and stem. Effects of these environmental signals on the activity of meristem have been largely explored. For example, local heating of the stem during the dormant period induces division of the cambium cell in the heated portions in some trees,15 suggesting that cell cycle progression can be driven by temperature signal. However the link between this environmental signal and cell cycle regulators in cambium cells is limited. Recently, the induction of PtoCDKB and PtoCYCB transcription by temperature provides insights into the molecular basis of the cell division machinery of cambium cells regulated by this environmental signal.6

Besides the roles in tree growth reactivation in spring,710 temperature also functions in dormancy induction in autumn and dormancy release in winter.11 In addition, natural chilling is required for the transition from rest (endodormancy) to quiescence (ecodormancy) in winter,12 and the induction of ABP1 (auxin binding protein 1) transcription.13 However, the molecular mechanism underlying the temperature regulation of dormancy remains scarce.

In poplar (Populus deltoides Bartr. ex Marsh.) and silver birch (Betula pendula Roth.), short days (SDs) alone induce growth cession and dormancy;14,15 while in apple (Malus pumila Mill.) and pear (Pyrus communis L.) low temperature, instead of photoperiod, controls growth cessation and dormancy induction.11 These indicate that the activities of meristem and cell cycle regulators are regulated by these environmental signals. For example, SD treatment results in the alteration of activities of the key cell cycle regulators at multiple levels.16 However, not all the cell cycle regulators are sensitive to the seasonal changes of environmental cues during the cycle of growth-dormancy, at least at the transcriptional levels. Analysis of the seasonal expression patterns of 68 potential cell cycle-related genes in aspen cambium cells by microarray hybridizations reveals that only 23 display significant changes during reactivation and 21 during the cessation of cell division.8 RT-PCR analysis of some cell cycle-related genes in early spring showed differential expression patterns in the P. tomentosa cambium region (Fig. 1). Besides CDKA, levels of CKS1, CYCD3, CDKB and CYCB homologue from P. tomentosa increased during cambium reactivation (Fig. 1). Given the effect of SD on PttCDKB transcription and the relationships between the annual change of daily air temperature and the seasonal expression patterns of PtoCDKB and PtoCYCB, it is concluded that the environmental signals may control the cycle of growth-dormancy of trees through regulating these key cell cycle genes.

Figure 1
expression patterns of cell cycle-related genes in the P. tomentosa cambium region assayed by RT-PCR in early 2008 using UBO-L as the internal control.

However it is still puzzling when considering the temperature regulation of some key cell cycle regulators. When the poplar trees are induced into endormancy (rest) under the controlled conditions, the PttCDKB expression is undetectable at both mRNA and protein levels.16 After transferring these endodormant trees into long day conditions for three months, the trees are unable to resume visible growth.16 Possibly, the functions of the core cell cycle regulators may not be reactivated in these trees under the long day conditions; is it because of the nonfulfillment of chilling requirement? Without chilling, dormant buds induced by SD in birch (Betula pubescens Ehrh.) remained dormant when grown in water culture under growth-promoting conditions.17 In view of these, low temperature (chilling) in winter is a prerequisite to promote the function of core cell cycle regulators through hitherto unknown mechanisms, and the induction of these regulators, such as PtoCDKB and PtoCYCB, by increasing temperature in spring is based on the fulfillment of chilling requirement in winter.

Hormonal regulation of the cycle of growth-dormancy of tree cambium and cell cycle genes has been largely investigated. It has been shown that the exogenous IAA is dispensable for PtoCDKB and PtoCYCB transcription in dormant cambium during water culture.6 In addition, ABA treatment also showed no distinct influence on PtoCDKB transcription under the same water culture conditions (Fig. 2). Meanwhile, one of the homologues of KRPs (kip-related cyclin-dependent kinase inhibitors)/ICKs (cyclin-dependent kinase inhibitors), among which ICK1 was inducible by ABA,18 in P. tomentosa became detectable after 3 weeks of water culture, whether or not exogenous ABA was present (Fig. 2), increasing complexity to understand the function of ABA in cambium dormancy. These results indicate that cues from water culture conditions apart from plant hormones play the main role in activating the transcription of these key cell cycle genes, and interaction between trigger and inhibitor of cell division is closely associated with the cycle of growth-dormancy of tree.

Figure 2
Variations of PtoCDKB and PtoKRP3 expression after water culture with exogenous ABA treatment. Cuttings were sampled on December 9 2005; after bud removal, they were cultured in water or ABA solution (50 µm) for 3 weeks. Variations of PtoCDKB ...

Taken together, environmental and hormonal regulation of cell cycle regulators is associated with growth-dormancy cycle of trees, and this can not be neglected when considering the impact of climate change on trees.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (30530620; 30670120; 30872001).

Footnotes

References

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