A key characteristic of plant development is its plasticity in response to various and dynamically changing environmental conditions. Tropisms contribute to this flexibility by allowing plant organs to grow from or towards environmental cues. Halotropism is a recently described tropism in which plant roots bend away from salt. During halotropism, as in most other tropisms, directional growth is generated through an asymmetric auxin distribution that generates differences in growth rate and hence induces bending. Here, we develop a detailed model of auxin transport in the Arabidopsis root tip and combine this with experiments to investigate the processes generating auxin asymmetry during halotropism. Our model points to the key role of root tip architecture in allowing the decrease in PIN2 at the salt-exposed side of the root to result in a re-routing of auxin to the opposite side. In addition, our model demonstrates how feedback of auxin on the auxin transporter AUX1 amplifies this auxin asymmetry, while a salt-induced transient increase in PIN1 levels increases the speed at which this occurs. Using AUX1-GFP imaging and pin1 mutants, we experimentally confirmed these model predictions, thus expanding our knowledge of the cellular basis of halotropism.

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Endocytosis and relocalization of auxin carriers represent important mechanisms for adaptive plant growth and developmental responses. Both root gravitropism and halotropism have been shown to be dependent on relocalization of auxin transporters. Following their homology to mammalian phospholipase Ds (PLDs), plant PLDζ‐type enzymes are likely candidates to regulate auxin carrier endocytosis. We investigated root tropic responses for an Arabidopsis pldζ1‐KO mutant and its effect on the dynamics of two auxin transporters during salt stress, that is, PIN2 and AUX1. We found altered root growth and halotropic and gravitropic responses in the absence of PLDζ1 and report a role for PLDζ1 in the polar localization of PIN2. Additionally, irrespective of the genetic background, salt stress induced changes in AUX1 polarity. Utilizing our previous computational model, we found that these novel salt‐induced AUX1 changes contribute to halotropic auxin asymmetry. We also report the formation of “osmotic stress‐induced membrane structures.” These large membrane structures are formed at the plasma membrane shortly after NaCl or sorbitol treatment and have a prolonged presence in a pldζ1 mutant. Taken together, these results show a crucial role for PLDζ1 in both ionic and osmotic stress‐induced auxin carrier dynamics during salt stress.

Priming is the process through which periodic elevations in auxin signalling prepattern future sites for lateral root formation, called prebranch sites. Thusfar is has remained a matter of debate to what extent elevations in auxin concentration and/or auxin signalling are critical for priming and prebranch site formation. Recently, we discovered a reflux-and-growth mechanism for priming generating periodic elevations in auxin concentration that subsequently dissipate. Here we reverse engineer a mechanism for prebranch site formation that translates these transient elevations into a persistent increase in auxin signalling, resolving the prior debate into a two-step process of auxin concentration mediated initial signal and auxin signalling capacity mediated memorization. A critical aspect of the prebranch site formation mechanism is its activation in response to time integrated rather than instantaneous auxin signalling. The proposed mechanism is demonstrated to be consistent with prebranch site auxin signalling dynamics, lateral inhibition and symmetry breaking mechanisms and perturbations in auxin homeostasis.

Auxin plays a major role in a variety of processes involved in plant developmental patterning and its adaptation to environmental conditions. Therefore, an important question is how specificity in auxin signalling is achieved, that is, how a single signalling molecule can carry so many different types of information. In recent years, many studies on auxin specificity have been published, unravelling increasingly more details on differential auxin sensitivity, expression domains and downstream partners of the auxin receptors (transport inhibitor response 1 (TIR1) and other auxin signaling F-box proteins (AFB)), transcriptional repressors that are degraded in response to auxin (AUX/IAA) and downstream auxin response factors (ARF) that together constitute the plant’s major auxin response pathways. These data are critical to explain how, in the same cells, different auxin levels may trigger different responses, as well as how in different spatial or temporal contexts similar auxin signals converge to different responses. However, these insights do not yet answer more complex questions regarding auxin specificity. As an example, they leave open the question of how similar sized auxin changes at similar locations result in different responses depending on the duration and spatial extent of the fluctuation in auxin levels. Similarly, it leaves unanswered how, in the case of certain tropisms, small differences in signal strength at both sides of a plant organ are converted into an instructive auxin asymmetry that enables a robust tropic response. Finally, it does not explain how, in certain cases, substantially different auxin levels become translated into similar cellular responses, while in other cases similar auxin levels, even when combined with similar auxin response machinery, may trigger different responses. In this review, we illustrate how considering the regulatory networks and contexts in which auxin signalling takes place helps answer these types of fundamental questions.