Parental shade stress increases Arabidopsis seed viability by modifying the phenolic hydrophobic barrier in the seed coats

Shade is a well-known environmental stressor that affects plant growth and development. However, little is understood about how parental shade stress impacts subsequent seed viability across generations. In this study, we exposed Arabidopsis plants to different shade signals, including reduced light quantity (RQ), reduced red/far-red ratio (RR), and a combination of both during the reproductive stage. While both RQ and RR treatments affected plant growth, only RR increased seed viability. Compared to seed coats developed under normal light conditions, the seed coats formed under RR conditions had a higher content and an altered composition of insoluble cell wall phenolics. By studying mutants impaired in the deposition of these phenolic polymers, we identified a positive relationship between the seed coat's insoluble phenolic content and seed viability. Further analysis found that seed coats with increased content of insoluble phenolic were less permeable, likely contributing to the higher seed viability. Taken together, we demonstrated that shade stress, particularly RR light conditions, during parental growth increases Arabidopsis seed viability by reducing seed coat permeability through the modification of its phenolic content and compositions. • Shade stress during the reproductive stage of Arabidopsis promotes the accumulation of phenolic polymers in the seed coats. • The increased accumulation of phenolic polymers leads to a reduction in seed coat permeability. • This reduced permeability enhances seed viability under deteriorative conditions. • These changes are induced by a decrease in the ratio of red to far-red light, rather than by a reduction in total light intensity.