A chemical genetic screen uncovers novel seed priming agents capable of persistent perturbation of anthocyanin regulation in Arabidopsis thaliana

Priming is a general term for a phenomenon in which exposure to an early environmental stimulus results in a more rapid or vigorous response when the plant is exposed to subsequent challenges. Various types of priming have been described: systemic acquired resistance against biotic stimuli, epigenetic stress memory induced by repeated abiotic stimuli, and seed priming treatments which apply water and additional adjuncts to seeds to improve crop performance. Using a high-throughput chemical genomic approach, thousands of small molecules were screened to identify compounds capable of chemical priming, asking if these could serve as artificial environments to persistently induce altered response to later abiotic challenges when applied as seed treatments. Attenuation of expected visual anthocyanin accumulation was chosen as a screening phenotype due to the visual nature of these pigments, as well as their biological roles in development and stress response. Several novel structural categories of molecules were identified that had the ability to reduce total anthocyanin accumulation in 7-18-day old seedlings induced by later low temperature challenge, persisting days after the removal of the compounds. Application variables were explored with thought to future use of the priming compounds as functional treatments: a dose-dependent relationship was established, additional effects on growth and development were documented to ensure minimal detrimental side effects on the treated plants, and the necessary temporal window of treatment was explored and reduced. Cross testing of the priming treatments identified by low temperature screening for ability to reduce anthocyanin induction by alternative exogenous and endogenous conditions showed consistent attenuative effect and revealed that the effect of priming on this metabolic phenotype was not specific to low temperature response. The presented research represents a proof-of-concept for the functional potential of seed priming with novel compounds, and highlights anthocyanin accumulation as a flexible component of plant stress response.