Rapid Auxin-Induced Cell Expansion and Gene Expression: A Four-Decade-Old Question Revisited

Schenck, Daniel; Christian, May; Jones, Alan M.; Lüthen, Hartwig

doi:10.1104/pp.109.149591

Cited by 67 publications

(57 citation statements)

References 17 publications

(16 reference statements)

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“…Root orientation of epidermal layers to the growth direction (twist angle) was quantified microscopically using agarose imprints as described (Wang et al, 2013). IAA-induced hypocotyl elongation was performed as described (Schenck et al, 2010). All experiments were performed at least in triplicate with 30 to 40 seedlings per each experiment.…”

Section: Plant Materials and Phenotypic Analysesmentioning

confidence: 99%

TWISTED DWARF1 Mediates the Action of Auxin Transport Inhibitors on Actin Cytoskeleton Dynamics

et al. 2016

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Plant growth and architecture is regulated by the polar distribution of the hormone auxin. Polarity and flexibility of this process is provided by constant cycling of auxin transporter vesicles along actin filaments, coordinated by a positive auxinactin feedback loop. Both polar auxin transport and vesicle cycling are inhibited by synthetic auxin transport inhibitors, such as 1-Nnaphthylphthalamic acid (NPA), counteracting the effect of auxin; however, underlying targets and mechanisms are unclear. Using NMR, we map the NPA binding surface on the Arabidopsis thaliana ABCB chaperone TWISTED DWARF1 (TWD1). We identify ACTIN7 as a relevant, although likely indirect, TWD1 interactor, and show TWD1-dependent regulation of actin filament organization and dynamics and that TWD1 is required for NPA-mediated actin cytoskeleton remodeling. The TWD1-ACTIN7 axis controls plasma membrane presence of efflux transporters, and as a consequence act7 and twd1 share developmental and physiological phenotypes indicative of defects in auxin transport. These can be phenocopied by NPA treatment or by chemical actin (de)stabilization. We provide evidence that TWD1 determines downstream locations of auxin efflux transporters by adjusting actin filament debundling and dynamizing processes and mediating NPA action on the latter. This function appears to be evolutionary conserved since TWD1 expression in budding yeast alters actin polarization and cell polarity and provides NPA sensitivity.

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Section: Plant Materials and Phenotypic Analysesmentioning

confidence: 99%

TWISTED DWARF1 Mediates the Action of Auxin Transport Inhibitors on Actin Cytoskeleton Dynamics

et al. 2016

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“…Whether this discrepancy is due to differences in species or assay conditions in unclear. Second, hypocotyl segments prepared from tir1 afb1 afb2 afb3 or tir1 afb2 afb3 seedlings were reported to elongate in response to auxin, albeit with delayed kinetics (Schenck et al, 2010;Fendrych et al, 2016). These seedlings lack three to four members of the six-member family of nuclear TIR1/AFB auxin receptors and exhibit a strong reduction in auxin-inducible gene expression (Dharmasiri et al, 2005), therefore suggesting that auxin-mediated SAUR expression may not be required for hypocotyl elongation.…”

Section: Constitutive Gfp-atsaur19 Expression Bypasses the Requiremenmentioning

confidence: 99%

Constitutive Expression of Arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in Tomato Confers Auxin-Independent Hypocotyl Elongation

et al. 2016

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The plant hormone indole-3-acetic acid (IAA or auxin) mediates the elongation growth of shoot tissues by promoting cell expansion. According to the acid growth theory proposed in the 1970s, auxin activates plasma membrane H + -ATPases (PM H + -ATPases) to facilitate cell expansion by both loosening the cell wall through acidification and promoting solute uptake. Mechanistically, however, this process is poorly understood. Recent findings in Arabidopsis (Arabidopsis thaliana) have demonstrated that auxin-induced SMALL AUXIN UP RNA (SAUR) genes promote elongation growth and play a key role in PM H + -ATPase activation by inhibiting PP2C.D family protein phosphatases. Here, we extend these findings by demonstrating that SAUR proteins also inhibit tomato PP2C.D family phosphatases and that AtSAUR19 overexpression in tomato (Solanum lycopersicum) confers the same suite of phenotypes as previously reported for Arabidopsis. Furthermore, we employ a custom image-based method for measuring hypocotyl segment elongation with high resolution and a method for measuring cell wall mechanical properties, to add mechanistic details to the emerging description of auxin-mediated cell expansion. We find that constitutive expression of GFP-AtSAUR19 bypasses the normal requirement of auxin for elongation growth by increasing the mechanical extensibility of excised hypocotyl segments. In contrast, hypocotyl segments overexpressing a PP2C.D phosphatase are specifically impaired in auxin-mediated elongation. The time courses of auxin-induced SAUR expression and auxindependent elongation growth were closely correlated. These findings indicate that induction of SAUR expression is sufficient to elicit auxin-mediated expansion growth by activating PM H + -ATPases to facilitate apoplast acidification and mechanical wall loosening.

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“…Accordingly, abp1-null mutant embryos have isodiametric cells that fail to elongate (Chen et al, 2001b), and downregulation of ABP1 in leaf tissues reduces the cell size (Braun et al, 2008). On the other hand, TIR1/AFBs do not seem to be involved in rapid cell expansion events, as multiple TIR1/AFB mutants still exhibit normal rapid elongation responses (Schenck et al 2010). A potential mechanism is that extracellular ABP1 is required for auxin-mediated hyperpolarization of the plasma membrane, which has been proven experimentally in several, independent systems (Barbier-Brygoo et al, 1989;Rü ck et al, 1993;Thiel et al, 1993;Bauly et al, 2000;Dahlke et al, 2010).…”

Section: Cell Expansionmentioning

confidence: 99%

AUXIN BINDING PROTEIN1: The Outsider

2011

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AUXIN BINDING PROTEIN1 (ABP1) is one of the first characterized proteins that bind auxin and has been implied as a receptor for a number of auxin responses. Early studies characterized its auxin binding properties and focused on rapid electrophysiological and cell expansion responses, while subsequent work indicated a role in cell cycle and cell division control. Very recently, ABP1 has been ascribed a role in modulating endocytic events at the plasma membrane and RHO OF PLANTS-mediated cytoskeletal rearrangements during asymmetric cell expansion. The exact molecular function of ABP1 is still unresolved, but its main activity apparently lies in influencing events at the plasma membrane. This review aims to connect the novel findings with the more classical literature on ABP1 and to point out the many open questions that still separate us from a comprehensive model of ABP1 action, almost 40 years after the first reports of its existence.

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Rapid Auxin-Induced Cell Expansion and Gene Expression: A Four-Decade-Old Question Revisited

Cited by 67 publications

References 17 publications

TWISTED DWARF1 Mediates the Action of Auxin Transport Inhibitors on Actin Cytoskeleton Dynamics

TWISTED DWARF1 Mediates the Action of Auxin Transport Inhibitors on Actin Cytoskeleton Dynamics

Constitutive Expression of Arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in Tomato Confers Auxin-Independent Hypocotyl Elongation

AUXIN BINDING PROTEIN1: The Outsider

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