Focus on circadian rhythms

In the 24 years since the first plant circadian oscillator genes were cloned (Schaffer et al., 1998; Wang and Tobin, 1998), there has been a concerted effort to identify the mechanistic basis of circadian rhythms and to understand how the circadian system impacts the biology of plants. Progress has been so great that there is now a good understanding of the circadian biology of Arabidopsis and insight into the circadian biology of the major crops is developing. For this Focus Issue on Circadian Rhythms, we encouraged submission of articles that emphasize less understood aspects, such as interactions between the circadian system and the natural environment, cell-specific function, setting of the circadian clock by environmental signals, and evolution of plant circadian oscillators. The Arabidopsis circadian oscillator was first modeled as a simple negative feedback loop, with two Myb-like transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), directly inhibiting expression of TIMING OF CAB EXPRESSION 1 (TOC1). TOC1, a member of the PSEUDO-RESPONSE REGULATOR family, was first proposed to promote CCA1 and LHY expression (Alabadi et al., 2001). However, later studies revealed that TOC1 directly represses CCA1 and LHY expression (Gendron et al., 2012; Huang et al., 2012; Pokhilko et al., 2012), with these three genes forming a double negative feedback loop. Subsequent work by many laboratories has revealed that the circadian oscillator mechanism in Arabidopsis is instead actually composed of dozens of genes that regulate each other’s expression, forming a very complex interconnected network (Nakamichi, 2020). Posttranslational regulation of circadian proteins is also pervasive, enhancing the robustness of the circadian system and fine-tuning circadian period (Yan et al., 2021). In addition to controlling each other’s expression, this slew of circadian oscillator transcription factors regulate a large fraction of the plant transcriptome, with up to 40% of Arabidopsis genes reported to be under circadian regulation (Romanowski et al., 2020). Given the widespread influence of circadian oscillators on gene expression, it is not surprising that many aspects of physiology, including photosynthesis, abiotic and biotic stress responses, and the transition from vegetative to reproductive growth are modulated by the circadian system (Sanchez and Kay, 2016). Indeed, breeding during domestication has selected for allelic variants in circadian clock genes in a large number of crop species (Steed et al., 2021; Maeda and Nakamichi, 2022). Future improvements in crop germplasm and agronomic practices will depend upon a better understanding of the circadian system and its interactions with the environment. While circadian clocks are present in most living organisms, they have independently arisen in different lineages (Jabbur and Johnson, 2022). In this issue, Peterson et al. provide an Update on recent advances in understanding the evolution of circadian components in the green lineage. Genomic surveys indicate deep conservation of core elements of circadian oscillators, not only in land plants but also in Chlorophyte and Charophyte algae. Moreover, Peterson and colleagues summarize our current understanding of the function of circadian components in several land plants and algae (Petersen et al., 2022). Maeda and Nakamichi (2022) provide an excellent Update covering human selection of varieties suited for local conditions (including photoperiod and other climatic features) which allowed the cultivation of plants outside the ecological range of their wild ancestors. These authors present examples from longday plants, such as wheat and barley, and short-day plants, such as rice and sorghum. How this process led to the selection of alleles that either flower early, or late, to avoid particularly dry, or wet times of the year, is well illustrated (Maeda and Nakamichi, 2022). Greenham et al. (2022) Ed it o ri al