Large-scale comparative transcriptomic analysis of temperature-responsive genes in Arabidopsis thaliana.

KEY MESSAGE: Comparative transcriptomic analysis provides broad and detailed understandings of transcriptional responses to a wide range of temperatures in different plant tissues, and unique regulatory functions of temperature-mediating transcription factors. Climate change poses a great threat to plant diversity and food security. It is thus of necessity to understand the molecular mechanisms for perceiving and responding to adverse temperature changes, to develop the cultivars that are resilient to these environmental stresses. Making use of publicly available datasets, we gathered and re-analyzed 259 individual transcriptomic profiles from 139 unique experiments of Arabidopsis thaliana's shoot, root, and seedling tissues, subjected to a wide variety of temperature conditions, ranging from freezing, cold, low and high ambient temperatures, to heat shock. Despite the underlying differences in the overall transcriptomic profiles between the plant tissues, we were able to identify distinct sets of genes whose transcription patterns were highly responsive to different types of temperature conditions, some were common among the tissues and some were tissue-specific. Interestingly, we observed that the known temperature-responsive genes such as the heat-shock factor (HSF) family, were up-regulated not only in response to high temperatures, but some of its members were also likely involved in the cold response. By integrating the DNA-binding specificity information of the key temperature transcription factor (TF) HSFA1a, PIF4, and CBFs, we elucidated their distinct DNA-binding patterns to the target genes that showed different transcriptional responses. Taken together, we have comprehensively characterized the transcription patterns of temperature-responsive genes and provided directly testable hypotheses on the regulatory roles of key temperature TFs on the expression dynamics of their target genes.

Exploring PIF4 's contribution to early flowering in plants under daily variable temperature and its tissue-specific flowering gene network.

Molecular mechanisms of how constant temperatures affect flowering time have been largely characterized in the model plant Arabidopsis thaliana; however, the effect of natural daily variable temperature outside laboratories is only partly explored. Several flowering genes have been shown to play important roles in temperature responses, including PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) and FLOWERING LOCUS C (FLC), the two genes encoding for the transcription factors (TFs) that act antagonistically to regulate flowering time by activating and repressing floral integrator FLOWERING LOCUS T (FT), respectively. In this study, we have taken a multidisciplinary approach to explore the contribution of PIF4 to the early flowering observed in the daily variable temperature (VAR) and to broaden its transcriptional network using publicly available transcriptomic data. We observed early flowering in the natural accessions Col-0, C24 and their late flowering hybrid C24xCol grown under VAR, as compared with a constant temperature (CON). The loss-of-function mutation of PIF4 exhibits later flowering in VAR in both the Col-0 parent and the C24xCol hybrid, suggesting that PIF4, at least in part, contributes to acceleration of flowering in the VAR condition. To investigate the interplay between PIF4 and its flowering regulator counterparts, FLC and FT, we performed transcriptional analyses and found that VAR increased PIF4 transcription at the end of the day when temperature peaked at 32°C, when FT transcription was also elevated. On the other hand, we observed a decrease in FLC transcription in the 4-week-old plants grown in VAR, as well as in the plants with PIF4 overexpression grown in CON. These results raise a possibility that PIF4 might also regulate FT indirectly through the repression of FLC, in addition to the well-characterized direct control of PIF4 over FT. To further expand our view on the PIF4-orientated flowering gene network in response to temperature changes, we have constructed a coexpression-transcriptional regulatory network by combining publicly available transcriptomic data and gene regulatory interactions of PIF4 and its closely related flowering genes, PIF5, FLC, and ELF3. The network model reveals conserved and tissue-specific regulatory functions, which are useful for confirming as well as predicting the functions and regulatory interactions between these key flowering genes.