Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes

Seeds use environmental cues to sense the seasons and their surroundings to initiate the life cycle of the plant. The dormancy cycling underlying this process is extensively described, but the molecular mechanism is largely unknown. To address this we selected a range of representative genes from published array experiments in the laboratory, and investigated their expression patterns in seeds of Arabidopsis ecotypes with contrasting life cycles over an annual dormancy cycle in the field. We show how mechanisms identified in the laboratory are coordinated in response to the soil environment to determine the dormancy cycles that result in winter and summer annual phenotypes. Our results are consistent with a seed-specific response to seasonal temperature patterns (temporal sensing) involving the gene DELAY OF GERMINATION 1 (DOG1) that indicates the correct season, and concurrent temporally driven co-opted mechanisms that sense spatial signals, i.e. nitrate, via CBL-INTERACTING PROTEIN KINASE 23 (CIPK23) phosphorylation of the NITRATE TRANSPORTER 1 (NRT1.1), and light, via PHYTOCHROME A (PHYA). In both ecotypes studied, when all three genes have low expression there is enhanced GIBBERELLIN 3 BETA-HYDROXYLASE 1 (GA3ox1) expression, exhumed seeds have the potential to germinate in the laboratory, and the initiation of seedling emergence occurs following soil disturbance (exposure to light) in the field. Unlike DOG1, the expression of MOTHER of FLOWERING TIME (MFT) has an opposite thermal response in seeds of the two ecotypes, indicating a role in determining their different dormancy cycling phenotypes.