Basally distributed actin array drives embryonic hypocotyl elongation during the seed‐to‐seedling transition in Arabidopsis

Abstract

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.

Cooperative actin filament nucleation by the Arp2/3 complex and formins maintains the homeostatic cortical array inArabidopsisepidermal cells

“…Several studies report that CK-666, a small molecule inhibitor of the Arp2/3 complex that is effective on yeast and animal cells ( Nolen et al 2009 ; Hetrick et al 2013 ), phenocopies the effects of arp2/3 mutants on tomato pollen tube growth ( Liu et al 2020 ) and Arabidopsis sperm nuclear migration ( Ali et al 2020 ), both of which depend upon the actin cytoskeleton. Moreover, a recent study demonstrates that CK-666 treatment does not influence actin redistribution between the basal and apical cell region in hypocotyl epidermal cells that occurs during early embryo growth ( Cui et al 2023 ). Because the earlier studies ( Ali et al 2020 ; Liu et al 2020 ) did not directly demonstrate the effects of CK-666 on actin organization or filament nucleation, it is necessary to validate whether CK-666 influences the function of the Arp2/3 complex in plant cells, as a side-branched actin filament nucleator, before we use it as an effective plant Arp2/3 inhibitor.…”

Cooperative actin filament nucleation by the Arp2/3 complex and formins maintains the homeostatic cortical array in Arabidopsis epidermal cells

“…Several studies report that CK-666, a small molecule inhibitor of the Arp2/3 complex that is effective on yeast and animal cells (Nolen et al, 2009; Hetrick et al, 2013), phenocopies the effects of arp2/3 mutants on tomato pollen tube growth (Liu et al, 2020) and Arabidopsis sperm nuclear migration (Ali et al, 2020), both of which depend upon the actin cytoskeleton. Moreover, a recent study demonstrates that CK-666 treatment does not influence actin redistribution between the basal and apical cell region in hypocotyl epidermal cells that occurs during early embryo growth (Cui et al, 2023). Because the earlier studies (Liu et al, 2020; Ali et al, 2020) did not directly demonstrate the effects of CK-666 on actin organization or filament nucleation, it is necessary to validate whether CK-666 influences the function of the Arp2/3 complex in plant cells, as a side-branched actin filament nucleator, before we use it as an effective plant Arp2/3 inhibitor.…”

Transmembrane formins as active cargoes of membrane trafficking

“…The effects of atfh1 mutations on pavement cell shaping can be interpreted as consequences of changes in actin and especially microtubule dynamics and arrangement rather than membrane trafficking (see also Cvrčková et al , 2016 ). The decreased hypocotyl elongation rate in young atfh1 seedlings has also been attributed to changes in actin organization ( Cui et al , 2023 ). In developing rice grains, loss of function or RNAi suppression of the class I formin OsFH15 led to decreased cell expansion in the spikelet hull tissues, resulting in smaller grain size, while OsFH15 overexpression facilitated spikelet hull tissue expansion, leading to larger grains.…”