Auxin and ROP GTPase Signaling of Polar Nuclear Migration in Root Epidermal Hair Cells

Abstract

ORCID IDs: 0000-0002-6456-1240 (T.G.); 0000-0002-0135-7533 (C.V.); 0000-0001-7571-0670 (M.G.).Polar nuclear migration is crucial during the development of diverse eukaryotes. In plants, root hair growth requires polar nuclear migration into the outgrowing hair. However, knowledge about the dynamics and the regulatory mechanisms underlying nuclear movements in root epidermal cells remains limited. Here, we show that both auxin and Rho-of-Plant (ROP) signaling modulate polar nuclear position at the inner epidermal plasma membrane domain oriented to the cortical cells during cell elongation as well as subsequent polar nuclear movement to the outer domain into the emerging hair bulge in Arabidopsis (Arabidopsis thaliana). Auxin signaling via the nuclear AUXIN RESPONSE FACTOR7 (ARF7)/ARF19 and INDOLE ACETIC ACID7 pathway ensures correct nuclear placement toward the inner membrane domain. Moreover, precise inner nuclear placement relies on SPIKE1 Rho-GEF, SUPERCENTIPEDE1 Rho-GDI, and ACTIN7 (ACT7) function and to a lesser extent on VTI11 vacuolar SNARE activity. Strikingly, the directionality and/or velocity of outer polar nuclear migration into the hair outgrowth along actin strands also are ACT7 dependent, auxin sensitive, and regulated by ROP signaling. Thus, our findings provide a founding framework revealing auxin and ROP signaling of inner polar nuclear position with some contribution by vacuolar morphology and of actin-dependent outer polar nuclear migration in root epidermal hair cells.

ACTIN7 Is Required for Perinuclear Clustering of Chloroplasts during Arabidopsis Protoplast Culture

“…This ability for ACT7 to show highly regulated expression is consistent with the strong upregulation of its expression during protoplast culture. A consequence of this variable expression is also that the various act7 mutants are defective in aspects of root growth and development [10,11]. Our quantitative gene expression analysis showed that ACT7 was the dominant ACT gene expressed across culture of wild-type protoplasts (Figure 4) and that the expression of ACT7 along with ACT8 partially compensated for the absence of ACT2 in the act2-1 mutant.…”

“…ACT7 mutants also show delayed germination and altered root growth, possibly explaining the strong selective disadvantage of act7-4 when grown in competition with wild-type plants [10]. Nuclear migration and positioning to establish polar outgrowth of root hairs requires ACT7 [11], whereas ACT2 is required for bulge site selection and tip growth [12]. Furthermore, an ACT2-dependent defect in root hair growth could not be complemented by overexpression of ACT7 in the act2 mutant [13].…”

Diurnal dynamics of the Arabidopsis rosette proteome and phosphoproteome

“…SnRK2.4 binds fatty acid derived lipid phosphatidic acid to associate with the plasma membrane (Julkowska et al, 2015) and responds to changes in cell osmotic status (Munnik et al, 1999), while SPK1, WDL5 and LARP1C are connected to plant hormone signaling through abscisic acid (WDL5; Yu et al, 2019), jasmonic acid (LARP1C; B. Zhang, Jia, Yang, Yan, & Han, 2012) and auxin (SPK1; Lin et al, 2012;Nakamura et al, 2018). Of these three proteins with concerted phosphorylation and abundance changes only SPK1 showed a parallel increase in abundance and phosphorylation at the same transition ( Figure 5), while WDL5 and LARP1C exhibited opposing patterns of phosphorylation and abundance changes, suggesting that phosphorylation may regulate their turnover.…”

Cellular Dynamics: Cellular Systems in the Time Domain

“…Knowledge about how the structure of the nucleus is generated and how it responds to developmental and biotic/abiotic signals is described in the Update by Groves et al (2018). The issue also contains an article that analyzes how nuclear position is controlled during root hair differentiation (Nakamura et al, 2018).…”