Zhejiang University: Crucial role of circadian clock in plant thermomorphogenesis

Global warming has a dramatic impact on plant ecosystems as well as on crop productivity. Plants are able to sense ambient temperatures and transduce these signals to trigger subsequent responses for physiological adjustment and developmental adaptation. Mild-warm temperatures induce morphological changes, including hypocotyl / petiole elongation, leaf hyponasty, and accelerated flowering, known as thermomorphogenesis. The circadian clock is an internal timekeeper that ensures growth, development, and fitness in a wide range of environmental conditions. How will the circadian clock regulate plant growth with the rise of temperature?

The research team led by LIU Jianxiang from the Zhejiang University College of Life Sciences published an article entitled “Timing to grow: roles of clock in thermomorphogenesis” in the August 14 issue of Trends in Plant Science.

The research highlights the molecular mechanism of the circadian clock in regulating plant growth in mild-warm temperatures. Thermosensors transduce temperature signals to the basic helix–loop–helix (bHLH) transcription factor PIF4 which promotes the expression of thermoresponsive genes and gets involved in regulating the formation of thermomorphogenesis. Morning expressed transcription factors CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY) repress the expression of afternoon PSEUDO-RESPONSE REGULATOR (PRR) genes such as PRR1/TIMING OF CAB EXPRESSION 1 (TOC1), PRR5, PRR7, and PRR9; in turn, TOC1 and other PRR proteins inhibit the expression of CCA1 and LHY, forming a negative feedback loop. CCA1 and LHY also repress the expression of evening genes encoding components in the evening complex (EC); again, EC represses the expression of afternoon PRR genes. REVEILLE 4/6/8 (RVE4/6/8), together with NIGHT LIGHT-INDUCIBLE AND CLOCK-REGULATED 1/2 (LNK1/2), are able to activate the expression of several clock genes including TOC1, PRR5, and EC components, but the expression of RVE8 is repressed by TOC1 and other PRRs, adding another complex of regulation in the network. Notably, CCA1/LHY are repressors and RVE4/RVE6/RVE8 are activators of gene expression. These factors combine to promote the rapid growth of plants at midnight at normal temperature.

The article also introduces the molecular mechanisms of EC and the components of EC in promoting the formation of plant thermomorphogenesis. EC is composed of EARLY FLOWERING (ELF3), EARLY FLOWERING 4 (ELF4) and LUX ARRHYTHMO (LUX, also known as PHYTOLOCK1). EC inhibits the expression of PIF4 in the evening. ELF3 alone can directly repress the transcriptional activity of PIF4 during the daytime. BBX18/23 recruit XBAT31/XBAT35 to ubiquitinate and degrade ELF3 at warm ambient temperatures, which releases the inhibitory effect of ELF3 on PIF4 activity and promotes plant growth. Because ELF3 is an important component of EC, the BBX18–XBAT31/XBAT35 regulatory module may also affect the protein stability of the whole EC at warm temperatures. In addition, PRRs’ inhibitory effect on PIF4 activity subdues at mild-warm temperatures. However, light intensity and mild-warm temperatures trigger the binding of CCA1/LHY and SHB1, thereby promoting the expression of PIF4. These factors contribute to the accelerated plant growth under long-day conditions and at mild-warm temperatures.

The article wraps up by putting forward some questions concerning the formation of plant thermomorphogenesis. “With these questions answered, the molecular mechanisms of plants in adapting to the rising ambient temperature will be further elucidated, thereby deepening our understanding of the regulatory effect of the circadian clock on plant growth,” said Liu. “It will be of immense significance to improve crop productivity and quality against the backdrop of global warming.”