AFC kinases function as thermosensors that regulate warm temperature-responsive growth in Arabidopsis

Roehl, B.; Ostwaldt, F.; Baesmann, J.; Hausmann, P.; Kreisz, P.; Krischke, M.; Lutsch, C.; Mueller, P. C.; Strauch, M.; Weiste, C.; Zhu, T.; De Smet, I.; Heyd, F.; Maag, D.

doi:10.1101/2024.06.21.600040

bioRxiv · 10.1101/2024.06.21.600040

AFC kinases function as thermosensors that regulate warm temperature-responsive growth in Arabidopsis

Roehl, B.·Ostwaldt, F.·Baesmann, J.·Hausmann, P.·Kreisz, P.·Krischke, M.·Lutsch, C.·Mueller, P. C.·Strauch, M.·Weiste, C.·Zhu, T.·De Smet, I.·Heyd, F.·Maag, D.

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Abstract

Plants respond to elevated temperatures with enhanced elongation growth that depends on rapid transcriptional, post-transcriptional, and post-translational reprogramming. However, it is unclear how temperature information integrates with the splicing machinery to establish warm temperature-dependent splicing patterns. In animals, CDC2-LIKE KINASES (CLKs) function as body temperature sensors that control temperature-dependent splicing via phosphorylation of serine/arginine-rich (SR) proteins. Here we demonstrate that the CLK-homologous ARABIDOPSIS FUS3-COMPLEMENTING (AFC) kinases likewise regulate post-transcriptional RNA processing to control warm temperature-dependent growth in Arabidopsis. The contrasting temperature-activity profiles of the three AFCs depend on specific structural elements, including a conserved activation segment within the kinase domain. Combining protein structure prediction with site-directed mutagenesis, we provide insights into structural features that determine the different temperature-activity profiles of the three AFC paralogs. Analyses of afc mutant plants demonstrate their role in establishing temperature-dependent splicing patterns and thermomorphogenic hypocotyl elongation. Finally, our data indicate SR34 and SR34a as phosphorylation targets mediating temperature-dependent hypocotyl elongation downstream of AFCs. In conclusion, our study provides evidence that temperature-controlled AFC activity is evolutionarily conserved between plants and animals and implicates AFCs in the control of thermomorphogenesis.

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Roehl, B., Ostwaldt, F., Baesmann, J., Hausmann, P., Kreisz, P., Krischke, M., Lutsch, C., Mueller, P. C., Strauch, M., Weiste, C., Zhu, T., De Smet, I., Heyd, F., Maag, D.. 2024-06-26. AFC kinases function as thermosensors that regulate warm temperature-responsive growth in Arabidopsis. https://doi.org/10.1101/2024.06.21.600040

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