Plants have evolved robust mechanisms to respond and adapt to unfavorable environmental conditions, such as low temperature. The C-repeat/drought-responsive element binding factor CBF1/DREB1b gene encodes a transcriptional activator transiently induced by cold that controls the expression of a set of genes responding to low temperature (the CBF regulon). Constitutive expression of CBF1 confers freezing tolerance but also slows growth. Here, we propose that low temperature-induced CBF1 expression restrains growth at least in part by allowing the accumulation of DELLAs, a family of nuclear growth-repressing proteins, the degradation of which is stimulated by gibberellin (GA). We show that cold/CBF1 enhances the accumulation of a green fluorescent protein (GFP)-tagged DELLA protein (GFP-RGA) by reducing GA content through stimulating expression of GA-inactivating GA 2-oxidase genes. Accordingly, transgenic plants that constitutively express CBF1 accumulate less bioactive GA and as a consequence exhibit dwarfism and late flowering. Both phenotypes are suppressed when CBF1 is expressed in a line lacking two DELLA proteins, GA-INSENSITIVE and REPRESSOR OF GA1-3. In addition, we show that DELLAs contribute significantly to CBF1-induced cold acclimation and freezing tolerance by a mechanism that is distinct from the CBF regulon. We conclude that DELLAs are components of the CBF1-mediated cold stress response.
Plant growth involves the integration of many environmental and endogenous signals that together with the intrinsic genetic program determine plant size. At the cellular level, growth rate is regulated by the combined activity of two processes: cell proliferation and expansion. Gibberellins (GA) are plant-specific hormones that play a central role in the regulation of growth and development with respect to environmental variability. It is well established that GA promote growth through cell expansion by stimulating the destruction of growth-repressing DELLA proteins (DELLAs); however, their effects on cell proliferation remain unknown. Kinematic analysis of leaf and root meristem growth revealed a novel function of DELLAs in restraining cell production. Moreover, by visualizing the cell cycle marker cyclinB1::beta-glucuronidase in GA-signaling mutants, we show that GA modulate cell cycle activity in the root meristem via a DELLA-dependent mechanism. Accordingly, expressing gai (a nondegradable DELLA protein) solely in root meristem reduced substantially the number of dividing cells. We also show that DELLAs restrain cell production by enhancing the levels of the cell cycle inhibitors Kip-related protein 2 (KRP2) and SIAMESE (SIM). Therefore, DELLAs exert a general plant growth inhibitory activity by reducing both cell proliferation and expansion rates, enabling phenotypic plasticity.
Gibberellins (GAs) are plant hormones involved in the regulation of plant growth in response to endogenous and environmental signals. GA promotes growth by stimulating the degradation of nuclear growth-repressing DELLA proteins. In Arabidopsis thaliana, DELLAs consist of a small family of five proteins that display distinct but also overlapping functions in repressing GA responses. This study reveals that DELLA RGA-LIKE3 (RGL3) protein is essential to fully enhance the jasmonate (JA)-mediated responses. We show that JA rapidly induces RGL3 expression in a CORONATINE INSENSITIVE1 (COI1)-and JASMONATE INSENSITIVE1 (JIN1/MYC2)-dependent manner. In addition, we demonstrate that MYC2 binds directly to RGL3 promoter. Furthermore, we show that RGL3 (like the other DELLAs) interacts with JA ZIM-domain (JAZ) proteins, key repressors of JA signaling. These findings suggest that JA/MYC2-dependent accumulation of RGL3 represses JAZ activity, which in turn enhances the expression of JA-responsive genes. Accordingly, we show that induction of primary JA-responsive genes is reduced in the rgl3-5 mutant and enhanced in transgenic lines overexpressing RGL3. Hence, RGL3 positively regulates JA-mediated resistance to the necrotroph Botrytis cinerea and susceptibility to the hemibiotroph Pseudomonas syringae. We propose that JA-mediated induction of RGL3 expression is of adaptive significance and might represent a recent functional diversification of the DELLAs.
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