Auxin-induced actin cytoskeleton rearrangements require AUX1.

Ruthie S Arieti,Christopher J Staiger

doi:10.1111/nph.16382

Abstract

Summary The actin cytoskeleton is required for cell expansion and implicated in cellular responses to the phytohormone auxin. However, the mechanisms that coordinate auxin signaling, cytoskeletal remodeling and cell expansion are poorly understood. Previous studies examined long‐term actin cytoskeleton responses to auxin, but plants respond to auxin within minutes. Before this work, an extracellular auxin receptor – rather than the auxin transporter AUXIN RESISTANT 1 (AUX1) – was considered to precede auxin‐induced cytoskeleton reorganization.In order to correlate actin array organization and dynamics with degree of cell expansion, quantitative imaging tools established baseline actin organization and illuminated individual filament behaviors in root epidermal cells under control conditions and after indole‐3‐acetic acid (IAA) application. We evaluated aux1 mutant actin organization responses to IAA and the membrane‐permeable auxin 1‐naphthylacetic acid (NAA).Cell length predicted actin organization and dynamics in control roots; short‐term IAA treatments stimulated denser and more parallel, longitudinal arrays by inducing filament unbundling within minutes. Although AUX1 is necessary for full actin rearrangements in response to auxin, cytoplasmic auxin (i.e. NAA) stimulated a lesser response.Actin filaments became more ‘organized’ after IAA stopped elongation, refuting the hypothesis that ‘more organized’ actin arrays universally correlate with rapid growth. Short‐term actin cytoskeleton response to auxin requires AUX1 and/or cytoplasmic auxin.

Highlights

Despite human dependence on plants for food, fiber, and fuel, we do not fully understand the molecular mechanisms controlling plant growth
Upon analyzing the actin arrays in two aux1 alleles, we found that actin failed to reorganize in response to indole-3-acetic acid (IAA) and actin reorganization was only partially restored by naphthylacetic acid (NAA)
We documented actin responses to growth-inhibitory doses of IAA and were surprised to find that filaments became more dense, parallel, and longitudinally oriented within 20–30 min, demonstrating that the relationship between higher levels of actin “organization” and increased cell expansion is not as direct as previously hypothesized

Summary

Introduction

Despite human dependence on plants for food, fiber, and fuel, we do not fully understand the molecular mechanisms controlling plant growth. Actin is accepted to provide tracks for vesicle delivery (Mathur, 2004; Hussey et al, 2006), but connections have been made between certain actin arrays and plant growth (ex., Nick et al, 2009; Higaki et al, 2010a; Smertenko et al, 2010; Dyachok et al, 2011; Yang et al, 2011, Yanagisawa et al, 2015), resulting in various hypotheses about actin’s role and/or the significance of specific actin arrays, each with a degree of supporting evidence, much of it circumstantial (Li et al, 2015a; Szymanski and Staiger, 2017)

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