Umeå University's logo

Plants align their physiology with daily environmental cycles through the circadian clock, which integrates light and metabolic signals to optimize growth and stress responses. While light entrainment has been extensively studied, emerging evidence highlights the central role of metabolism—particularly from chloroplasts and mitochondria—in tuning circadian rhythms. In this review, we explore the bidirectional relationship between organelle metabolism and the circadian clock, focusing on how metabolic signals such as sugars, ROS, and organic acids function as entrainment cues. We discuss how the clock regulates organelle function at multiple levels, including transcriptional, translational, and post-translational mechanisms, and how organelle-derived signals feedback to modulate core clock components through retrograde pathways. Special attention is given to the integration of chloroplast and mitochondrial signals, emphasizing their synergistic roles in maintaining cellular homeostasis. Drawing on the “three-body problem” analogy, we illustrate the dynamic and reciprocal interactions among light, clock, and metabolism. This perspective underscores the need to reframe the circadian system, not merely as light-driven but also as a central integrator of energy status and environmental cues. Understanding this integrated network is essential to improve plant performance and resilience under fluctuating environmental conditions.

Retrograde signalling networks originating in the organelles dictate nuclear gene expression and are essential for control and regulation of cellular energy metabolism. We investigate whether such plastid retrograde signals control nuclear gene expression by altering the chromatin state during the establishment of photosynthetic function in response to light. An Arabidopsis thaliana cell culture provides the required temporal resolution to map four histone modifications during the greening process. We uncover sequential and distinct epigenetic reprogramming events where an epigenetic switch from a histone methylation to an acetylation at photosynthesis-associated loci is dependent on a plastid retrograde signal. The transcription factors VIVIPAROUS1/ABI3-LIKE (VAL1), RELATIVE OF EARLY FLOWERING 6 (REF6) and GOLDEN2-LIKE FACTOR1/2 (GLKs) are linked to the H3K27ac deposition at photosynthesis associated loci that precedes full activation of the photosynthesis genes. Our work demonstrates that retrograde signals play a role in the epigenetic reprogramming essential to the establishment of photosynthesis in plant cells.

The components of the mediator kinase module are highly conserved across all eukaryotic lineages, and cyclin-dependent kinase 8 (CDK8) is essential for correct cell proliferation and differentiation in diverse eukaryotic systems. We show that CDK8 couples leaf development with the establishment of correct stomata patterning for prevailing CO₂ conditions. In Arabidopsis, the basic helix-loop-helix (bHLH) transcription factor SPEECHLESS (SPCH) controls cellular entry into the stomatal cell lineage, and CDK8 interacts with and phosphorylates SPCH, controlling SPCH protein levels and thereby also expression of the SPCH target genes encoding key regulators of cell fate and asymmetric cell divisions. The lack of the CDK8-mediated control of SPCH results in an increased number of meristemoid and guard mother cells, and increased stomata index in the cdk8 mutants. Increasing atmospheric CO₂ concentrations trigger a developmental programme controlling cell entry into stomatal lineage by limiting the asymmetric divisions. In cdk8, the number of meristemoids and guard mother cells remains the same under ambient and high CO₂ concentrations, as the accumulated levels of SPCH caused by the lack of CDK8 appear to override the negative regulation of increased CO₂. Thus, our work provides novel mechanistic understanding of how plants alter critical leaf properties in response to increasing atmospheric CO₂.

The development of a seedling into a photosynthetically active plant is a crucial process. Despite its importance, we do not fully understand the regulatory mechanisms behind the establishment of functional chloroplasts. We herein provide new insight into the early light response by identifying the function of three basic region/leucine zipper (bZIP) transcription factors: bZIP16, bZIP68, and GBF1. These proteins are involved in the regulation of key components required for the establishment of photosynthetically active chloroplasts. The activity of these bZIPs is dependent on the redox status of a conserved cysteine residue, which provides a mechanism to finetune light-responsive gene expression. The blue light cryptochrome (CRY) photoreceptors provide one of the major light-signaling pathways, and bZIP target genes overlap with one-third of CRY-regulated genes with an enrichment for photosynthesis/chloroplast-associated genes. bZIP16, bZIP68, and GBF1 were demonstrated as novel interaction partners of CRY1. The interaction between CRY1 and bZIP16 was stimulated by blue light. Furthermore, we demonstrate a genetic link between the bZIP proteins and cryptochromes as the cry1cry2 mutant is epistatic to the cry1cry2bzip16bzip68gbf1 mutant. bZIP16, bZIP68, and GBF1 regulate a subset of photosynthesis associated genes in response to blue light critical for a proper greening process in Arabidopsis.