Temperature variability is integrated by a spatially embedded decision-making center to break dormancy in Arabidopsis seeds

Significance Both plants and animals make decisions in response to the environment to maximize their fitness. Plants use dormancy in seeds to move through time and space, and timing of the transition to germination is influenced by external cues, including temperature. Here, we report the presence of a decision-making center within the root tip of dormant seeds and demonstrate that it shares a similar configuration as some systems within the human brain. Unlike in humans, where this spatial structure is used to filter out noisy inputs from the environment, seeds use this arrangement to harness fluctuating temperatures and stimulate the termination of dormancy. Variable inputs therefore act as an instructive signal for seeds, enhancing the accuracy with which plants are established in ecosystems. Plants perceive and integrate information from the environment to time critical transitions in their life cycle. Some mechanisms underlying this quantitative signal processing have been described, whereas others await discovery. Seeds have evolved a mechanism to integrate environmental information by regulating the abundance of the antagonistically acting hormones abscisic acid (ABA) and gibberellin (GA). Here, we show that hormone metabolic interactions and their feedbacks are sufficient to create a bistable developmental fate switch in Arabidopsis seeds. A digital single-cell atlas mapping the distribution of hormone metabolic and response components revealed their enrichment within the embryonic radicle, identifying the presence of a decision-making center within dormant seeds. The responses to both GA and ABA were found to occur within distinct cell types, suggesting cross-talk occurs at the level of hormone transport between these signaling centers. We describe theoretically, and demonstrate experimentally, that this spatial separation within the decision-making center is required to process variable temperature inputs from the environment to promote the breaking of dormancy. In contrast to other noise-filtering systems, including human neurons, the functional role of this spatial embedding is to leverage variability in temperature to transduce a fate-switching signal within this biological system. Fluctuating inputs therefore act as an instructive signal for seeds, enhancing the accuracy with which plants are established in ecosystems, and distributed computation within the radicle underlies this signal integration mechanism.