Unlocking allelic variation in circadian clock genes to develop environmentally robust and productive crops

Abstract

Molecular mechanisms of biological rhythms provide opportunities to harness functional allelic diversity in core (and trait- or stress-responsive) oscillator networks to develop more climate-resilient and productive germplasm. The circadian clock senses light and temperature in day-night cycles to drive biological rhythms. The clock integrates endogenous signals and exogenous stimuli to coordinate diverse physiological processes. Advances in high-throughput non-invasive assays, use of forward- and inverse-genetic approaches, and powerful algorithms are allowing quantitation of variation and detection of genes associated with circadian dynamics. Circadian rhythms and phytohormone pathways in response to endogenous and exogenous cues have been well documented the model plant Arabidopsis. Novel allelic variation associated with circadian rhythms facilitates adaptation and range expansion, and may provide additional opportunity to tailor climate-resilient crops. The circadian phase and period can determine adaptation to environments, while the robustness in the circadian amplitude can enhance resilience to environmental changes. Circadian rhythms in plants are tightly controlled by multiple and interlocked transcriptional-translational feedback loops involving morning (CCA1, LHY), mid-day (PRR9, PRR7, PRR5), and evening (TOC1, ELF3, ELF4, LUX) genes that maintain the plant circadian clock ticking. Significant progress has been made to unravel the functions of circadian rhythms and clock genes that regulate traits, via interaction with phytohormones and trait-responsive genes, in diverse crops. Altered circadian rhythms and clock genes may contribute to hybrid vigor as shown in Arabidopsis, maize, and rice. Modifying circadian rhythms via transgenesis or genome-editing may provide additional opportunities to develop crops with better buffering capacity to environmental stresses. Models that involve clock gene‒phytohormone‒trait interactions can provide novel insights to orchestrate circadian rhythms and modulate clock genes to facilitate breeding of all season crops.

Keywords: Adaptation; Allelic variation; Biological rhythms; Breeding all season crops; Clock genes and signaling; Heterosis; Non-invasive assays; Stress tolerance.

Fig. 1

Circadian oscillator components. A Extended model representation of the components of the circadian oscillator. B Simplified model representation of the components of the circadian oscillator. Solid black lines ending with dashes represent the transcriptional repression. C Graphic representation between the hormonal response and the circadian oscillator. The relative timing of action to every component is illustrated in the upper part of the extended model, from left to right during a day–night cycle. Transcriptional repressors are filled in dark blue colour, while transcriptional activators are filled in green colour. Solid lines represent direct regulatory effects while dashed lines represent indirect (or possibly direct but not experimentally determined) effects. Black lines ending with dashes represent the transcriptional repression; green lines ending with arrows represent the transcriptional activation. The circadian repressor components are Circadian Clock Associated 1 (CCA1); Late Elongated Hypocotyl (LHY); Timing of CAB2 Expression 1 (TOC1); Pseudo-Response Regulator 9 (PRR9), PRR7 and PRR5; evening complex (EC) components formed by LUX Arrhythmo (LUX) or Brother of LUX Arrhythmo (BOA), Early Flowering 3 (ELE3), and ELE4; Cold-Regulated 27 (COR27) and COR28; CCA1 Hiking Expedition (CHE). The circadian activation components are Reveille (RVEs); Night Light-Inducible and Clock-Regulated 1 (LNK1), and LNK2; Light-Regulated WD1 (LWD1) and LWD2; Teosinte Branched1-Cycloidea-PCE 20 (TCP20), and TCP22. Proteins involved in brassinosteroids (BRs) circadian regulations are bri1-EMS-Suppressor 1 (BES1) and Topless (TPL). Proteins involved in the Abscisic acid (ABA) circadian regulation are biosynthesis 9-cis-epoxycarotenoid dioxygenase enzymes 3 (NCED3) and MYB96. In the Jasmonic acid (JA) circadian regulation, a basic helix-loop-helix-leucine zipper transcription factor (MYC2) is a key component. Regarding auxin regulation, RVE1 (a member of the RVE transcription factor family but not involved in the core circadian regulation) as well as the auxin biosynthetic gene YUCCA8 (YUC8) are involved

Fig. 2

Effect of circadian allelic variations in the adaptation to different latitudes. Allelic variations linked to the adaptation for production in high-latitude (short-season and long-photoperiod) environments in Solanum lycopersicum (tomato); Hordeum vulgare (barley) and Triticum sp. (wheat)

Fig. 3

Circadian component effects under abiotic stress condition. This figure represents the effect of the mutation/silencing or overexpression of the circadian genes in the tolerance to different abiotic stresses. Solid lines represent direct regulatory effects while dashed lines represent indirect (or possibly direct but not experimentally determined) effects. Black lines ending with dashes represent the transcriptional repression of the circadian oscillator components. Green lines ending with arrows represent the transcriptional activation of the circadian oscillator components. Red lines ending with dashes represent transcriptional repression from or to the inputs and outputs in regard to the circadian oscillator. Blue lines ending with arrows represent transcriptional activation from or to the inputs and outputs regarding the circadian oscillator. The circadian repressor components in Arabidopsis are Circadian Clock Associated 1 (CCA1); Late Elongated Hypocotyl (LHY); Timing of CAB2 Expression 1 (TOC1); Pseudo-Response Regulator 9 (PRR9), PRR7 and PRR5; evening complex (EC). The circadian activation components in Arabidopsis are Reveille (RVEs); Night light-iducible and clock-regulated (LNKs); Light-regulated WD (LWDs); Teosinte Branched1-Cycloidea-PCE (TCPs). In Rice, OsCCA1 seems to transcriptionally activate protein phosphatase 2C (OsPP2C) and leucine zipper 46 (OsbZIP46), which have been shown to cope with the negative effects of ROS, drought, and salinity. OsPRR73 inhibit the High-affinity K + transporter 2;1 (OsHKT2;1) which is a negative factor in conferring tolerance to saline conditions. Similarly, the receptor for activated C kinase 1A (OsRACK1A) is circadian regulated and has been shown to have a negative effect increasing the sensitivity to salinity

Fig. 4

The circadian oscillator in plants: integrating environmental and physiological cues to improve adaptation and resilience. The intricate circadian oscillator in plants continually integrates environmental and physiological cues, including signals from phytohormones, natural environments, and abiotic stress conditions. The oscillator responds to these inputs with coordinated output signals, allowing the plant to adjust its physiology and behaviour accordingly. Recent research has revealed that natural allelic variations or induced mutations in genes involved in the regulation of the circadian oscillator can significantly impact how plants perceive inputs or regulate outputs, ultimately leading to improved adaptation to new environments, enhanced tolerance to abiotic stress, and increased crop yields. This figure highlights the importance of understanding the genetic and molecular mechanisms underlying the circadian oscillator’s regulation and how they can be manipulated to improve plant performance and resilience