Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis

Increasing global temperatures have an impact on flowering, and the underlying mechanisms are just beginning to be unravelled(1,2). Elevated temperatures can induce flowering, and different mechanisms that involve either activation or de-repression of FLOWERING LOCUS T (FT) by transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) or the FLOWERING LOCUS M (FLM)-SHORT VEGETATIVE PHASE (SVP) complex, respectively, have been suggested to be involved(3-6). Thermosensitivity in flowering has been mapped to FLM(5), which encodes a floral repressor(7,8). FLM undergoes alternative splicing(8) and it has been suggested that temperature-dependent alternative splicing leads to differential accumulation of the FLM-β and FLM-δ transcripts, encoding proteins with antagonistic effects, and that their ratio determines floral transition(4). Here we show that high temperatures downregulate FLM expression by alternative splicing coupled with nonsense-mediated mRNA decay (AS-NMD). We identify thermosensitive splice sites in FLM and show that the primary effect of temperature is explained by an increase in NMD target transcripts. We also show that flm is epistatic to pif4, which suggests that most of the PIF4 effects are FLM dependent. Our findings suggest a model in which the loss of the floral repressor FLM occurs through mRNA degradation in response to elevated temperatures, signifying a role for AS-NMD in conferring environmental responses in plants.