Understanding the genetic factors involved in seed longevity is of paramount importance in agricultural and ecological contexts. The polygenic nature of this trait suggests that many of them remain undiscovered. Here, we exploited the contrasting seed longevity found amongst Arabidopsis thaliana accessions to further understand this phenomenon. Concentrations of glutathione were higher in longer‐lived than shorter‐lived accessions, supporting that redox poise plays a prominent role in seed longevity. However, high seed permeability, normally associated with shorter longevity, is also present in long‐lived accessions. Dry seed transcriptome analysis indicated that the contribution to longevity of stored messenger RNA (mRNAs) is complex, including mainly accession‐specific mechanisms. The detrimental effect on longevity caused by other factors may be counterbalanced by higher levels of specific mRNAs stored in dry seeds, for instance those of heat‐shock proteins. Indeed, loss‐of‐function mutant analysis demonstrated that heat‐shock factors HSF1A and 1B contributed to longevity. Furthermore, mutants of the stress‐granule zinc‐finger protein TZF9 or the spliceosome subunits MOS4 or MAC3A/MAC3B, extended seed longevity, positioning RNA as a novel player in the regulation of seed viability. mRNAs of proteins with putative relevance to longevity were also abundant in shorter‐lived accessions, reinforcing the idea that resistance to ageing is determined by multiple factors.

During flowering plant reproduction, anthers produce pollen grains, the development of which is supported by the tapetum, a nourishing maternal tissue that also contributes non-cell-autonomously to the pollen wall, the resistant external layer on the pollen surface. How the anther restricts movement of the tapetum-derived pollen wall components, while allowing metabolites such as sugars and amino acids to reach the developing pollen, remains unknown. Here, we show experimentally that in arabidopsis thaliana the tapetum and developing pollen are symplastically isolated from each other, and from other sporophytic tissues, from meiosis onwards. We show that the peritapetal strip, an apoplastic structure, separates the tapetum and the pollen grains from other anther cell layers and can prevent the apoplastic diffusion of fluorescent proteins, again from meiosis onwards. The formation and selective barrier functions of the peritapetal strip require two NADPH oxidases, RBOHE and RBOHC, which play a key role in pollen formation. Our results suggest that, together with symplastic isolation, gating of the apoplast around the tapetum may help generate metabolically distinct anther compartments.