The time of day effects of warm temperature on flowering time involve PIF4 and PIF5

Authors: THINES, BRYAN - University Of California; YOUNGWON, YOUN - University Of California; DUARTE, MARITZA - University Of California; Harmon, Frank

Submitted to: Journal of Experimental Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/9/2013
Publication Date: 3/30/2014
Citation: Thines, B.C., Youngwon, Y., Duarte, M.I., Harmon, F.G. 2014. The time of day effects of warm temperature on flowering time involve PIF4 and PIF5. Journal of Experimental Botany. 65(4):1141-51. DOI: 10.1093/jxb/ert487.

Interpretive Summary: Plants are very sensitive to their temperature environment. Climate change is modifying the historic temperature profile in many parts world that are important for agriculture. Therefore, it is critical to understand how plants sense and respond to their temperature environment. The signaling pathways for temperature perception are largely unknown. In many plant species, a warm temperature like 28°C triggers earlier flowering compared to a moderate temperature like 22°C. The model plant Arabidopsis thaliana has this behavior. This study evaluated when Arabidopsis plants sense warm temperature cues in relation to day and night, as well as the genes needed for warm temperature to cause earlier flowering. While warm temperature present during any part of the photocycle elicited earlier flowering, the magnitude of the early flowering response was unequal between 28°C warm days (WD) and 28°C warm nights (WN). In general, plants given the WN treatment flowered earlier than WD grown plants. Several signaling pathways were involved in this response and the precise combination of pathways employed depended on the time of the temperature cue. Important genes for the WN-promoted flowering were the well-established flowering time genes CO and FT. Unexpectedly, flowering in WD did not appear to involve these genes; instead, uncharacterized pathways acted to make plants flower. A novel discovery was that the transcription factors PIF4 and PIF5 were required for warm temperature-induced flowering. This study shows that these transcription factors act together to match floral development with the combined light and temperature environment.

Technical Abstract: To probe the signaling pathways that promote early flowering under warm temperatures, the flowering time of Arabidopsis thaliana plants was evaluated in day-neutral photocycles that had warm temperature (28°C) added during the day, night, or both. Warm temperature present during any part of the photocycle elicited earlier flowering. Multiple signaling pathways were involved in the flowering response and these pathways relied to varying degrees on the CO, FT, PIF4 and PIF5 genes. Plants exposed to 28°C warm nights (WN) flowered sooner than those held in constant 22°C control conditions, an effect comparable to 28°C constant warm (CW) conditions. Treatment with 28°C warm day (WD) conditions also induced flowering, but WD grown plants initiated flowering later than in WN and CW. FT expression was highly upregulated in WN grown plants and the rhythmic expression waveform of CO was advanced to earlier in the day. Plants in WD showed no stimulation of FT expression and suppression of CO expression late in the day. Unexpectedly, WN conditions induced earlier expression PIF4 and PIF5, but WD and CW did not. pif4-2, pif5-3, and pif4-2 pif5-3 mutants were late flowering in all temperature conditions. Therefore, PIF5 and PIF4 are redundant floral activators and these genes act together in at least two pathways: one responsible for induction of FT expression in WN conditions and a second activated by WD that appeared to be independent of changes in FT expression. These results show that Arabidopsis plants discriminate the timing of warm temperature cues and employ different sets of floral regulators to stimulate flowering, including novel genes like PIF4 and PIF5.