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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.

Boreal forests are dominated by evergreen conifers that show strongly regulated seasonal photosynthetic activity. Understanding the mechanisms behind seasonal modulation of photosynthesis is crucial for predicting how these forests will respond to changes in seasonal patterns and how this will affect their role in the terrestrial carbon cycle. We demonstrate that the two co-occurring dominant boreal conifers, Scots pine (Pinus sylvestris L.) and Norway spruce (Picea abies), use contrasting mechanisms to reactivate photosynthesis in the spring. Scots pine downregulates its capacity for CO₂ assimilation during winter and activates alternative electron sinks through accumulation of PGR5 and PGRL1 during early spring until the capacity for CO₂ assimilation is recovered. In contrast, Norway spruce lacks this ability to actively switch between different electron sinks over the year and as a consequence suffers severe photooxidative damage during the critical spring period.