Summary: How the biophysical properties of overlaying tissues control growth, such as the embryonic root (radicle) during seed germination, is a fundamental question. In eudicot seeds the endosperm surrounding the radicle confers coat dormancy and controls germination responses through modulation of its cell wall mechanical properties. Far less is known for grass caryopses that differ in tissue morphology. Here we report that the coleorhiza, a sheath‐like organ that surrounds the radicle in grass embryos, performs the same role in the grass weed Avena fatua (common wild oat). We combined innovative biomechanical techniques, tissue ablation, microscopy, tissue‐specific gene and enzyme activity expression with the analysis of hormones and oligosaccharides. The combined experimental work demonstrates that in grass caryopses the coleorhiza indeed controls germination for which we provide direct biomechanical evidence. We show that the coleorhiza becomes reinforced during dormancy maintenance and weakened during germination. Xyloglucan endotransglycosylases/hydrolases may have a role in coleorhiza reinforcement through cell wall remodelling to confer coat dormancy. The control of germination by coleorhiza‐enforced dormancy in grasses is an example of the convergent evolution of mechanical restraint by overlaying tissues.

SUMMARY: Underdeveloped (small) embryos embedded in abundant endosperm tissue, and thus having morphological dormancy (MD) or morphophysiological dormancy (MPD), are considered to be the ancestral state in seed dormancy evolution. This trait is retained in the Apiaceae family, which provides excellent model systems for investigating the underpinning mechanisms. We investigated Apium graveolens (celery) MD by combined innovative imaging and embryo growth assays with the quantification of hormone metabolism, as well as the analysis of hormone and cell‐wall related gene expression. The integrated experimental results demonstrated that embryo growth occurred inside imbibed celery fruits in association with endosperm degradation, and that a critical embryo size was required for radicle emergence. The regulation of these processes depends on gene expression leading to gibberellin and indole‐3‐acetic acid (IAA) production by the embryo and on crosstalk between the fruit compartments. ABA degradation associated with distinct spatiotemporal patterns in ABA sensitivity control embryo growth, endosperm breakdown and radicle emergence. This complex interaction between gibberellins, IAA and ABA metabolism, and changes in the tissue‐specific sensitivities to these hormones is distinct from non‐MD seeds. We conclude that the embryo growth to reach the critical size and the associated endosperm breakdown inside MD fruits constitute a unique germination programme.

Main conclusion: Storage at an elevated partial pressure of oxygen and classical artificial ageing cause a rapid loss of seed viability of short-lived vegetable seeds. Prolonging seed longevity during storage is of major importance for gene banks and the horticultural industry. Slowing down biochemical deterioration, including oxygen-dependent deterioration caused by oxidative processes can boost longevity. This can be affected by the seed structure and the oxygen permeability of seed coat layers. Classical artificial seed ageing assays are used to estimate seed 'shelf-life' by mimicking seed ageing via incubating seeds at elevated temperature and elevated relative humidity (causing elevated equilibrium seed moisture content). In this study, we show that seed lots of vegetable Allium species are short-lived both during dry storage for several months and in seed ageing assays at elevated seed moisture levels. Micromorphological analysis of the Allium cepa x Allium fistulosum salad onion seed identified intact seed coat and endosperm layers. Allium seeds equilibrated at 70% relative humidity were used to investigate seed ageing at tenfold elevated partial pressure of oxygen (high pO₂) at room temperature (22 ºC) in comparison to classical artificial ageing at elevated temperature (42 ºC). Our results reveal that 30 days high pO₂ treatment causes a rapid loss of seed viability which quantitatively corresponded to the seed viability loss observed by ~ 7 days classical artificial ageing. A similar number of normal seedlings develop from the germinating (viable) proportion of seeds in the population. Many long-lived seeds first exhibit a seed vigour loss, evident from a reduced germination speed, preceding the loss in seed viability. In contrast to this, seed ageing of our short-lived Allium vegetable seems to be characterised by a rapid loss in seed viability.