Plants exhibit an acute sensitivity to thermal fluctuations, with even a 1°C variation capable of significantly influencing their growth and developmental trajectories. Unlike the stress responses elicited by extreme thermal conditions, the adaptive reactions of plants to ambient temperature changes (ranging from 12°C to 27°C) necessitate a distinct set of mechanisms. Within the arsenal of identified components, Thermosensory Transcription Factors (TTFs) assume a central role in facilitating warm temperature (for instance, 27°C)-driven elongation of the hypocotyl (the embryonic stem), a phenomenon described as thermomorphogenesis. Among the various TTF families identified thus far, PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) stands out for its crucial function in steering thermomorphogenetic expansion. Once activated in response to elevated temperatures, PIF4 enhances hypocotyl elongation by upregulating critical genes engaged in the synthesis and signaling pathways of auxin, a pivotal growth hormone. Through forward and reverse genetic approaches and bioinformatic analyses, we have identified multiple factors that may contribute to the regulation of PIF4 expression, activity, and protein stability in response to temperature elevations.
Funded by the National Science Foundation, #2239963 (2023-2028)
The function of the Mediator co-activator complex in thermomorphogenesis
The Mediator complex, a pivotal co-activator, is indispensable for the majority of, if not all, transcriptional processes mediated by RNA Polymerase II (Pol II). It engages in critical interactions with Pol II and gene-specific transcription activators via its head and tail modules, respectively, thereby acting as a crucial conduit that enables the assembly of the pre-initiation complex. Our research has illuminated that PIF4, alongside its co-activator HEMERA (HMR), enlists the Mediator complex for the activation of thermo-induced, growth-promoting genes through direct interactions with the tail subunit MED14. This finding prompts the hypothesis that other TTFs, akin to PIF4, may similarly engage with MED14 and additional tail subunits (such as MED25) to drive the expression of genes responsive to thermal changes. Our objective is to employ thermomorphogenesis as a paradigm to explore the dynamic interplay between the Mediator complex and transcriptional regulators, thereby delineating the intricate mechanism through which MED14 integrates the actions of various TTFs in response to a singular environmental cue—elevated temperatures. This approach aims to provide a comprehensive understanding of the transcriptional orchestration underlying plant responses to warm temperatures.
Publications:
Qiu, Y., Li, M., Kim, R.J., Moore, C., Chen, M. (2019) Daytime temperature is sensed by phytochrome B in Arabidopsis through a transcriptional activator HEMERA. Nat Commun 10: 140. PDF
Bajracharya A, Xi J, Grace KF, Bayer EE, Grant CA, Clutton CH, Baerson SR, Agarwal AK, Qiu Y (2022) PIF4/HEMERA-mediated thermosensory growth requires the Mediator subunit MED14. Plant Physiol 2022, kiac412, https://doi.org/10.1093/plphys/kiac412 PDF
PIF4 protein stability control at warm temperatures is crucial for thermomorphogenesis
PIF4 proteins are subject to regulation by the ubiquitin-proteasome system (UPS), which targets them for degradation. Notably, the stabilization of PIF4 proteins under warm conditions is facilitated by both an upsurge in transcriptional activity and a mechanism that impedes their degradation. The identification of a weak allele of HMR, designated as hmr-22, has been instrumental in elucidating the latter process. Despite normal thermo-induced transcriptional levels of PIF4, the hmr-22 mutant exhibits a marked inability to sustain PIF4 protein levels at elevated temperatures. A suppressor screen of hmr-22 has led to the discovery of multiple suppressor mutants capable of rectifying the thermomorphogenetic shortcomings observed in hmr-22 under higher thermal conditions (for instance, at 27°C). By analyzing these suppressors, our research is poised to decipher the precise regulatory mechanisms governing PIF4 protein stability in response to increased ambient temperatures.
Publications
Qiu, Y.*†, Pasoreck, E.K.*, Yoo, C.Y.*, He, J., Wang, H., Bajracharya, A., Li, M., Larsen, H.D., Cheung, S., Chen, M.† (2021) RCB initiates Arabidopsis thermomorphogenesis by stabilizing the thermoregulator PIF4 in the daytime. Nat Commun 12: 2042. († Co-corresponding authors; * Co-first authors) PDF
Identification of the gene regulatory network in plant thermomorphogenesis
Via forward genetic screens, we have pinpointed several novel TTF families potentially playing substantial roles in thermosensory hypocotyl elongation. Alongside established TTF families — including PIF, BBX, TCP, HSF, and BZR, which are integral to plant thermomorphogenesis — the challenge now lies in integrating these critical transcription regulators to form a holistic understanding of the gene regulatory network governing plant thermomorphogenesis. We are in the process of investigating their cell-type-specific functions using single-cell RNA-sequencing technology. The forthcoming phase of our research is dedicated to synthesizing these disparate strands into a cohesive framework, aiming to elucidate the complex orchestration of genetic controls that facilitate plant responses to thermal cues. This endeavor seeks to map out the intricate web of interactions and regulatory mechanisms that underpin the dynamic process of plant thermomorphogenesis.
Publications:
Qiu, Y. (2020) Regulation of PIF4-mediated thermosensory growth. Plant Sci 297: 110541. PDF
Qiu Laboratory at Ole Miss 