Phytochrome-imposed inhibition of PIF7 activity shapes photoperiodic growth in Arabidopsis together with PIF1, 3, 4 and 5

Authors: LEIVAR, PABLO - University Of California; MARTIN, GUIOMAR - University Of California; SOY, JUDIT - University Of California; DALTON-ROESLER, JUTTA - University Of California; QUAIL, PETER - University Of California; MONTE, ELENA - University Of California

Submitted to: Physiologia Plantarum
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2020
Publication Date: 7/1/2020
Citation: Leivar, P., Martin, G., Soy, J., Dalton-Roesler, J., Quail, P., Monte, E. 2020. Phytochrome-imposed inhibition of PIF7 activity shapes photoperiodic growth in Arabidopsis together with PIF1, 3, 4 and 5. Physiologia Plantarum. 169(3):452-466. https://doi.org/10.1111/ppl.13123.
DOI: https://doi.org/10.1111/ppl.13123

Interpretive Summary: Phytochrome interacting factors (PIFs) are basic helix–loop–helix transcriptional regulators that are promoters of elongation growth in Arabidopsis thaliana. PIFs interact specifically with the active Pfr conformer of phytochrome (phy) photoreceptors. In the dark, the phy inactive red (R) light-absorbing Pr conformer is localized in the cytosol and PIFs accumulate in the nucleus. Upon light exposure, phy Pr converts to the biologically active far red (FR) light-absorbing Pfr form, which translocates into the nucleus and interacts with the PIFs, triggering rapid degradation of the PIF quartet (PIFq) members PIF1, PIF3, PIF4 and PIF5 (with half-lives of 5–20 min). Here, by genetic analysis of pif7 mutants, we show that PIF7 is a prominent target of phyB-mediated suppression of growth at night, when it promotes growth in SD and especially under SD-EODFR conditions.

Technical Abstract: Under photoperiodic conditions, Arabidopsis thaliana seedling growth is inhibited in long days (LDs), but promoted under the extended nights of short days (SDs). This behavior is partly implemented by phytochrome (phy)-imposed oscillations in the abundance of the growth-promoting, phy-interacting bHLH transcription factors PHY-INTERACTING FACTOR 1 (PIF1), PIF3, PIF4 and PIF5 (PIF quartet or PIFq). However, the observation that a pifq mutant is still stimulated to elongate when given a phy-inactivating end-of-day far-red pulse (EODFR), suggests that additional factors are involved in the phy-mediated suppression of growth during the subsequent dark period. Here, by combining growth-analysis of pif7 single- and higher-order mutants with gene expression analysis under SD, LD, SD-EODFR, and LD-EODFR, we show that PIF7 promotes growth during the dark hours of SD, by regulating growth-related gene expression. Interestingly, the relative contribution of PIF7 in promoting growth is stronger under EODFR, whereas PIF3 role is more important under SD, suggesting that PIF7 is a prominent target of phy-suppression. Indeed, we show that phy imposes phosphorylation and inactivation of PIF7 during the light hours in SD and prevents full dephosphorylation during the night. This repression can be lifted with an EODFR, which correlates with increased PIF7-mediated gene expression and elongation. In addition, our results suggest that PIF7 function might involve heterodimerization with PIF3. Furthermore, our data indicate that a pifqpif7 quintuple mutant is largely insensitive to photoperiod for hypocotyl elongation. Collectively, the data suggest that PIF7, together with the PIFq, is required for the photoperiodic regulation of seasonal growth.