A PHOT2-NPH3-CAMTA2 light-temperature coincidence detection system in Arabidopsis I

Light and temperature variations are inescapable in nature, providing many types of information and influencing development and physiology. PHOTOTROPIN (PHOT) blue light receptor-kinases play well-characterized roles in multiple processes in short time scales, but functions over days, weeks, or seasons have rarely been explored. Here we show that PHOT2 integrates blue light and low temperature signals to control leaf number at flowering. Plants lacking PHOT2 show delayed flowering, specifically when grown in low temperature. This effect is blocked by loss of NON-PHOTOTROPIC HYPOCOTYL 3 (NPH3), and can be phenocopied by reduced blue light intensity, and by removal of CAMTA2. PHOT2 and CAMTA2 show non-additive genetic interactions, and a deep RNA-sequencing time course reveals highly overlapping phot2- and camta2-dependent effects on gene expression patterns across the day. Network-based co-expression analysis indicates system-level up-regulation of key growth modules in phot2 and camta2 mutants. Temperature- and genotype-dependent modulation of florigen-anti-florigen balance in phot2 and camta2 mutants is consistent with the phenotype. Together these data establish PHOT2 and NPH3 as a light-temperature coincidence detection module, operating with CAMTA2 as a downstream or parallel regulator of PHOT2-dependent gene expression. Overall design: We aimed to understand temperature-dependent molecular links between PHOTOTROPIN2 and CAMTA2,and functions of these genes over daily cycles. Arabidopsis thaliana plants (gl1 (background control), phot1-5 gl1, and phot2-1 gl1) were germinated on 1/2x Linsmaier & Skoog medium, transplanted to soil two days after germinating, and moved to growth chambers under 16h light:8h dark cycles, light intensity ~100µmol m-2 s-1 at 20°C and 15°C. Shoot tissue (above ground) from three plants per sample was harvested at ZT16 (just prior to lights-off) and ZT24 (just prior to the following lights-on) of day 14. Each genotype, temperature, and timepoint was collected in biological duplicate.