MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis (miRNA-Seq)

MicroRNAs (miRNAs) play diverse roles in plant development, but whether and how miRNAs participate in thermomorphogenesis remains ambiguous. Here we show that HYPONASTIC LEAVES1 (HYL1) – a key component of microRNA biogenesis – acts downstream of the thermal regulator PHYTOCHROME INTERACTING FACTOR 4 in temperature-dependent plasticity of hypocotyl growth in Arabidopsis. A hyl1-2 suppressor screen identified a dominant dicer-like1 (dcl1) allele, dcl1-24, which rescues hyl1-2's defects in miRNA biosynthesis and warm temperature-induced hypocotyl elongation. Genome-wide miRNA and transcriptome analysis reveal microRNA156 (miR156) and its target SQUAMOSA PROMOTER-BINDING-LIKE 9 (SPL9) as critical regulators of thermomorphogenesis. Surprisingly, perturbation of the miR156/SPL9 module disengages seedling responsiveness to warm temperatures by impeding auxin sensitivity. Moreover, the miR156-dependent auxin sensitivity also operates in the shade avoidance response at lower temperatures. Thus, these results unveil the miRNA156/SPL9 module as a previously-uncharacterized genetic circuitry that enables plant growth plasticity in response to environmental temperature and light changes. Overall design: We compared global miRNA levels in 4-d-old Col-0, hyl1-2 and dcl1-24/hyl1-2 seedlings grown in 50 umol m-2 s-1 red light at either 21 C or 27 C.