This article presents a detailed model for the regulation of lateral root formation in Arabidopsis thaliana seedlings grown in culture. We demonstrate that direct contact between the aerial tissues and sucrose in the growth media is necessary and sufficient to promote emergence of lateral root primordia from the parent root. Mild osmotic stress is perceived by the root, which then sends an abscisic acid-dependent signal that causes a decrease in the permeability of aerial tissues; this reduces uptake of sucrose from the culture media, which leads to a repression of lateral root formation. Osmotic repression of lateral root formation in culture can be overcome by mutations that cause the cuticle of a plant's aerial tissues to become more permeable. Indeed, we report here that the previously described lateral root development2 mutant overcomes osmotic repression of lateral root formation because of a point mutation in Long Chain Acyl-CoA Synthetase2, a gene essential for cutin biosynthesis. Together, our findings (1) impact the interpretation of experiments that use Arabidopsis grown in culture to study root system architecture; (2) identify sucrose as an unexpected regulator of lateral root formation; (3) demonstrate mechanisms by which roots communicate information to aerial tissues and receive information in turn; and (4) provide insights into the regulatory pathways that allow plants to be developmentally plastic while preserving the essential balance between aboveground and belowground organs.

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Seasonal behavior is important for fitness in temperate environments but it is unclear how progeny gain their initial seasonal entrainment. Plants use temperature signals to measure time of year, and changes to life histories are therefore an important consequence of climate change. Here we show that in Arabidopsis the current and prior temperature experience of the mother plant is used to control germination of progeny seeds, via the activation of the florigen Flowering Locus T (FT) in fruit tissues. We demonstrate that maternal past and current temperature experience are transduced to the FT locus in silique phloem. In turn, FT controls seed dormancy through inhibition of proanthocyanidin synthesis in fruits, resulting in altered seed coat tannin content. Our data reveal that maternal temperature history is integrated through FT in the fruit to generate a metabolic signal that entrains the behavior of progeny seeds according to time of year.M any organisms use annual changes in temperature to control their phenology, resulting in predictable timing of key life history events, such as flowering, spawning, and migration (1-3). Understanding crop and ecosystem response to climate change requires knowledge of the temperature control of key developmental transitions, but how new generations achieve seasonal orientation is currently unclear. Seed germination is the first step in plant life history and therefore plays a central role in the control of plant phenology (4) and is extremely sensitive to environmental temperature (3-5). Seed dormancy is established during seed maturation and is imposed by control of hormone signaling and the action of the maternal seed coat. Nearly 30 y ago it was found that environmental signaling throughout the whole maternal life history can affect seed dormancy control in wild oats, and that temperature experience in the vegetative phase before flowering affected progeny seed dormancy (6). Here we show that this response is conserved on the model species Arabidopsis. Our data show that fruit tissues carry a memory of past temperature experience and that flowering pathways control a transgenerational metabolic signal of maternal past temperature experience, which modulates progeny dormancy according to time of year.To test whether past parental temperature experience affected progeny dormancy in the model species Arabidopsis thaliana, we grew plants until the first sign of flowering at either 22°C or 16°C and then placed plants side by side to set seed at 22°C in long days (LDs) (Fig. 1A). We found that in Landsberg erecta (Ler) lower temperature during the vegetative phase caused a large increase in the dormancy of seeds produced later on the plants (Fig. 1A). Lower temperatures during seed set also increase progeny dormancy (6), but we observed no effect of photoperiod on dormancy either before or after flowering, as has been reported previously (7, 8). Therefore, temperature signals before seed fertilization are remembered by the parent plant and used to control offspring behavior.P...

Clock-regulated pathways coordinate the response of many developmental processes to changes in photoperiod and temperature. We model two of the best-understood clock output pathways in Arabidopsis, which control key regulators of flowering and elongation growth. In flowering, the model predicted regulatory links from the clock to CYCLING DOF FACTOR 1 (CDF1) and FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) transcription. Physical interaction data support these links, which create threefold feed-forward motifs from two clock components to the floral regulator FT. In hypocotyl growth, the model described clock-regulated transcription of PHYTOCHROME-INTERACTING FACTOR 4 and 5 (PIF4, PIF5), interacting with post-translational regulation of PIF proteins by phytochrome B (phyB) and other light-activated pathways. The model predicted bimodal and end-of-day PIF activity profiles that are observed across hundreds of PIF-regulated target genes. In the response to temperature, warmth-enhanced PIF4 activity explained the observed hypocotyl growth dynamics but additional, temperature-dependent regulators were implicated in the flowering response. Integrating these two pathways with the clock model highlights the molecular mechanisms that coordinate plant development across changing conditions.