Summary Seed germination is a vital developmental transition for the production of progeny by sexual reproduction in spermatophytes. The seed‐to‐seedling transition is predominately driven by hypocotyl cell elongation. However, the mechanism that underlies hypocotyl growth remains largely unknown. In this study, we characterized the actin array reorganization in embryonic hypocotyl epidermal cells. Live‐cell imaging revealed a basally organized actin array formed during hypocotyl cell elongation. This polarized actin assembly is a barrel‐shaped network, which comprises a backbone of longitudinally aligned actin cables and a fine actin cap linking these cables. We provide genetic evidence that the basal actin array formation requires formin‐mediated actin polymerization and directional movement of actin filaments powered by myosin XIs. In fh1‐1 and xi3ko mutants, actin filaments failed to reorganize into the basal actin array, and the hypocotyl cell elongation was inhibited compared with wild‐type plants. Collectively, our work uncovers the molecular mechanisms for basal actin array assembly and demonstrates the connection between actin polarization and hypocotyl elongation during seed‐to‐seedling transition.
Precise control over how and where actin filaments are created in eukaryotic cells leads to the construction of unique cytoskeletal arrays with specific functions within a common cytoplasm. Actin filament nucleators are key players in this activity and include the conserved Actin-Related Protein 2/3 (Arp2/3) complex, that creates dendritic networks of branched filaments, as well as a large family of formins that typically generate long, unbranched filaments and bundles. In some eukaryotic cells, these nucleators compete for a common pool of actin monomers and loss of one favors the activity of the other. To test whether this is a common mechanism across kingdoms, we combined the ability to image single filament dynamics in living plant epidermal cells with genetic and/or small molecule inhibitor approaches to stably or acutely disrupt nucleator activity. We found that Arp2/3 mutants or acute CK-666 treatment markedly reduced the frequency of side-branched nucleation events as well as overall actin filament abundance. We also confirmed that plant formins contributed to side-branched filament nucleation in vivo. Surprisingly, simultaneous inhibition of both nucleators increased overall actin filament abundance and enhanced the frequency of de novo nucleation events. Collectively, these observations suggest that plant cells have a unique actin filament nucleation mechanism compared to yeast or animal cells.
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