Temperature-dependent polar lignification of a seed coat suberin layer promoting dormancy in Arabidopsis thaliana

Abstract

The seed is a landmark plant adaptation where the embryo is sheltered by a protective seed coat to facilitate dispersion. In Arabidopsis, the seed coat, derived from ovular integuments, plays a critical role in maintaining dormancy, ensuring germination occurs during a favorable season. Dormancy is enhanced by cold temperatures during seed development by affecting seed coat permeability through changes in apoplastic barriers. However, the localization and composition of these apoplastic barriers are poorly understood. This study identifies and investigates a polar barrier in the seed coats outer integument (oi1) cells. We present histological, biochemical, and genetic evidence showing that cold promotes polar seed coat lignification of the outer integument 1 (oi1) cells and suberization throughout the entire oi1 cell boundary. The polar oi1 barrier is regulated by the transcription factors MYB107 and MYB9. MYB107, in particular, is crucial for the lignified polar oi1 barrier formation under cold temperatures. The absence of the oi1 barrier in mutant seeds correlates with increased permeability and reduced dormancy. Our findings elucidate how temperature-induced modifications in seed coat composition regulate dormancy, highlighting the roles of suberin and lignin in this process. Significance statementOur study uncovers how cold temperatures during seed development in the mother plant influence seed dormancy through apoplastic modifications in the Arabidopsis thaliana seed coat. We identified a polar lignin barrier in the outer integument 1 (oi1) cells, which are also suberized. Lignification and suberization are regulated by transcription factors MYB107 and MYB9. Cold promotes lignification and suberization of oi1 cells through MYB107, thus creating a "memory" that reduces seed permeability and strengthens dormancy. Mutants defective in the oi1 barrier exhibit lower dormancy, highlighting the adaptive importance of this barrier. These findings advance our understanding of temperature-induced seed coat adaptations and their agricultural implications, particularly in the context of climate change, offering valuable insights for improving crop resilience and yield.