Long-term high temperatures affect seed maturation and seed coat integrity in Brassica napus

Temperatures above the optimum growth threshold affect seed development, accelerating embryo development and producing seeds with ruptured seed coats. However, the underlying mechanisms of this effect remain unclear. To investigate temperature-induced seed coat rupture, we used a multidisciplinary approach combining detailed phenotyping, transcriptomics, histology, immunolabelling, cell wall profiling and nanoindentation-based mechanics of the seed coat in oilseed rape (Brassica napus). Our data reveal that high temperatures accelerate embryo growth, resulting in larger embryos without a compensatory increase in overall seed size. This rapid embryo expansion may exert elevated mechanical stress on the seed coat cells, significantly thinning the seed coat layers. Concurrently, prolonged exposure to high temperatures drives premature biochemical maturation of the seed coat, characterized by accumulation of demethylesterified pectin. Nanoindentation analysis demonstrated that these changes may have compromised the structural integrity of seed coat cell walls. Ultimately, the weakened seed coat may not withstand the internal tension imposed by the fast-growing embryo, leading to seed coat rupture and reduced seed quality. Our work on seed maturation and the mechanism of heat-induced seed coat rupture provides valuable insights for future research into breeding thermotolerant Brassica napus, crucial in the context of a changing climate. HIGHLIGHTSO_LIGrowth of Brassica napus under long-term high temperatures accelerated embryo growth and led to seed coat rupture in approximately half of the seeds. C_LIO_LIPathways linked to cell wall modification were found to be significantly differentially regulated at high temperatures, accompanied by increased pectin demethylesterification in the seed coat. C_LIO_LIA lower reduced modulus and hardness indicate that the surface of HT seeds is mechanically more compliant and softer. Together with the reduced thickness of the seed coat layers, such a seed coat, as a whole structure, is mechanically weaker and less able to resist deformation imposed by embryo growth, resulting in seed coat rupture. C_LI