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Integration of low temperature and light signaling during cold acclimation response in Arabidopsis

AuthorsCatalá, Rafael ; Medina, Joaquín; Salinas, Julio
Issue Date27-Sep-2011
PublisherNational Academy of Sciences (U.S.)
CitationProceedings of the National Academy of Sciences 108(39):16475-16480(2011)
AbstractCertain plants increase their freezing tolerance in response to low nonfreezing temperatures, an adaptive process named cold acclimation. Light has been shown to be required for full cold acclimation, although how light and cold signals integrate and cross-talk to enhance freezing tolerance still remains poorly understood. Here, we show that HY5 levels are regulated by low temperature transcriptionally, via a CBF- and ABA-independent pathway, and posttranslationally, via protein stabilization through nuclear depletion of COP1. Furthermore, we demonstrate that HY5 positively regulates cold-induced gene expression through the Z-box and other cis-acting elements, ensuring the complete development of cold acclimation. These findings uncover unexpected functions for HY5, COP1, and the Z-box in Arabidopsis response to low temperature, provide insights on how cold and light signals integrate to optimize plant survival under freezing temperatures, and reveal the complexity of the molecular mechanisms plants have evolved to respond and adapt to their fluctuating natural environment.
Plants have evolved a variety of adaptive mechanisms to survive adverse environmental conditions. In the case of freezing temperatures, which negatively affect plant growth and distribution, and affect crop quality and productivity, some species are able to increase their tolerance after low-nonfreezing temperature exposure, an adaptive process termed cold acclimation (1). External signals, however, cannot be considered in isolation when studying the adaptive responses plants have evolved to survive in an ever-changing environment. Plants must process and integrate the surrounding signals to adequately respond to changes in their environmental conditions. The correct integration of low temperature and light signals, for instance, is crucial to ensure the appropriate development of cold acclimation. Thus, light is required for the increase in freezing tolerance that is produced during cold acclimation in Arabidopsis (2). The role of light in cold acclimation seems to be mediated through the phytochromes (3) and would consist in positively regulating cold-induced gene expression (4, 5). Consistent with these results, expression analysis in Arabidopsis have revealed that light is required for cold induction of several genes involved in cold acclimation, including CBFs (5, 6). Interestingly, light quality has also been described to have a function in regulating plant freezing tolerance. A low red to far-red ratio light signal increases CBF expression in Arabidopsis, this increase being sufficient to confer freezing tolerance at temperatures higher than those required for cold acclimation (7). All these studies evidence a complex cross-talk between light and low temperature signals in the regulation of cold acclimation. The pathways and molecular components that mediate such a cross-talk, however, still remain largely unknown
HY5 is an Arabidopsis bZIP transcription factor that has a pivotal role in light signaling, mediating photoreceptor responses to promote photomorphogenesis (8). In additon, it has also been described to mediate plant responses to UV-B (9) and to different hormones, such as ABA, gibberellins, cytokinin, and auxins (8). Recently, a ChIP-chip approach has revealed that HY5 recognizes several light-responsive elements, including the Z-box, and binds >9,000 genes, detectably affecting the expression of >1,100 targets (10). Further, HY5 indirectly regulates many other genes through subnetworks mediated by other regulators (10). Therefore, HY5 seems to be one of the central modulators of gene expression for the coordination of light signals and plant development. Consistent with this relevant function, HY5 levels are strongly regulated. At the transcriptional level, HY5 expression is positively regulated by light via a phytochrome-dependent pathway (11). Posttranslationally, HY5 is regulated by the E3 ubiquitin ligase COP1, a crucial repressor of light signaling. In the dark, it is turned over in the nucleus by COP1 (12). In the light, COP1 is excluded from the nucleus, allowing HY5 increase stabilization and activation of light-responsive genes (12). COP1 has also been shown to be depleted from the nucleus in response to giberellins and cytokinin (8). Intriguingly, however, although COP1 is not excluded from the nucleus in response to UV-B, HY5 is not degraded (9).
We reported that the expression of CAB1, an Arabidopsis light-regulated gene, is induced by cold, indicating that CAB1 constitutes a common intermediate of Arabidopsis responses to light and low temperature (13). To further understand the complex integration of cold and light signaling, we have investigated the molecular mechanisms underlying the cold induction of CAB1. Here, we show that the induction of CAB1 in response to low temperature is mediated by HY5 through the Z-box, which constitutes a low temperature responsive element (LTRE). Our results demonstrate that, in addition to CAB1, HY5 mediates the induction of ≈10% of all Arabidopsis cold-inducible genes, including those involved in anthocyanin biosynthesis, ensuring the complete development of cold acclimation. Interestingly, we also demonstrate that HY5 levels are regulated by low temperature transcriptionally, via a CBF- and ABA-independent pathway, and posttranslationally, via protein stabilization through the nuclear depletion of COP1. These data indicate that HY5, COP1, and the Z-box integrate cold and light signaling to promote the cold acclimation response
Description6 páginas, 6 figuras -- PAGS nros. 16475-16480
Publisher version (URL)http://dx.doi.org/10.1073/pnas.1107161108
Appears in Collections:(CIB) Artículos
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