Demonsais, L. | bioRxiv Science

bioRxiv2024

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

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.

plant biology↗

bioRxiv2020

Tannic cell walls form a continuous apoplastic barrier sustaining Arabidopsis seed coat biophysical properties

Seeds are a late land plant evolution innovation that promoted the striking spread and diversity of angiosperms. The seed coat is a specialized dead tissue protecting the plant embryo from mechanical damage. In many species, including Arabidopsis thaliana, the seed coat also achieves a remarkable balancing act: it limits oxygen uptake, avoiding premature embryo oxidative damage, but not entirely so as to enable seed dormancy release. The seed coat biophysical features implementing the striking physiological properties of the seed remain poorly understood. Tannins, a type of flavonoids, are antioxidants known to accumulate in the Arabidopsis seed coat and transparent testa (tt) mutant seeds, deficient in flavonoid synthesis, exhibit low dormancy and viability. However, their precise contribution to seed coat architecture and biophysics remains evasive. A seed coat cuticle, covering the endosperm outer surface was, intriguingly, previously shown to be more permeable in tt mutants deficient not in cuticular component synthesis, but rather in flavonoid synthesis. Investigating the role of flavonoids in cuticle permeability led us to identify cell walls, originating from the seed coat inner integument 1 cells, impregnated with tannins. We found that tannic cell walls are tightly associated with the cuticle, forming two fused layers that regulate endosperm permeability. In addition, we show that tannic cell walls are prominent building blocks of the seed coat, constituting a continuous barrier around the seed living tissues. Altogether our findings reveal the existence of tannic cell walls as a previously unrecognized biological barrier sustaining the seeds key physiological properties. One sentence summaryThe seed coat is largely composed of plant cell walls impregnated with tannins, forming a thick and continuous protective barrier surrounding the embryo promoting seed viability and dormancy.

plant biology↗