The 5'-3' mRNA Decay Pathway Modulates The Plant Circadian Network In Arabidopsis.

Circadian rhythms enable organisms to anticipate and adjust their physiology to periodic environmental changes. These rhythms are controlled by biological clocks that consist of a set of clock genes that regulate each other's expression. Circadian oscillations in mRNA levels require regulation of mRNA production and degradation. While transcription factors controlling clock function have been well characterised from cyanobacteria to humans, the role of factors controlling mRNA decay is largely unknown. Here, we show that mutations in LSM1 and XRN4, components of the 5'-3' mRNA decay pathway, alter clock function in Arabidopsis. We found that lsm1 and xrn4 mutants display long-period phenotypes for clock gene expression. In xrn4, these circadian defects were associated with changes in circadian phases of expression, but not overall mRNA levels, of several core clock genes. We then used non-invasive transcriptome-wide mRNA stability analysis to identify genes and pathways regulated by XRN4. Among genes affected in the xrn4 mutant at the transcriptional and post-transcriptional level, we found an enrichment in genes involved in auxin, ethylene, and drought recovery. Large effects were not observed for canonical core-clock genes, although the mRNAs of several auxiliary clock genes that control the pace of the clock, were stabilised in xrn4 mutants. Our results establish that the 5'-3' mRNA decay pathway constitutes a novel post-transcriptional regulatory layer of the circadian gene network, which probably acts through a combination of small effects on mRNA stability of several auxiliary and some core clock genes.