In response to gravity stimulation, the PIN3 auxin transporter polarizes to the bottom side of gravity-sensing root cells, presumably redirecting the auxin flux toward the lower side of the root and triggering gravitropic bending. By combining live-cell imaging techniques with pharmacological and genetic approaches, we demonstrate that PIN3 polarization does not require secretion of de novo synthesized proteins or protein degradation, but instead involves rapid, transient stimulation of PIN endocytosis, presumably via a clathrin-dependent pathway. Our data suggest that gravity perception acts at several instances of PIN3 trafficking, ultimately leading to the polarization of PIN3, which presumably aligns auxin fluxes with gravity vector and mediates downstream root gravitropic response. Keywords: polarity, exocytosis, gravitropism, plant cell biology Plants have evolved a profound phenotypic plasticity, enabling growth to adapt to changes in environmental conditions. The complex developmental reprogramming often involves resetting of developmental fate and polarity of cells within differentiated tissues.
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In response to gravity stimulation, the PIN3 auxin transporter polarizes to the bottom side of gravity-sensing root cells, presumably redirecting the auxin flux toward the lower side of the root and triggering gravitropic bending.
By combining live-cell imaging techniques with pharmacological and genetic approaches, we demonstrate that PIN3 polarization does not require secretion of de novo synthesized proteins or protein degradation, but instead involves rapid, transient stimulation of PIN endocytosis, presumably via a clathrin-dependent pathway.
Our data suggest that gravity perception acts at several instances of PIN3 trafficking, ultimately leading to the polarization of PIN3, which presumably aligns auxin fluxes with gravity vector and mediates downstream root gravitropic response.
Keywords: polarity, exocytosis, gravitropism, plant cell biology Plants have evolved a profound phenotypic plasticity, enabling growth to adapt to changes in environmental conditions. The complex developmental reprogramming often involves resetting of developmental fate and polarity of cells within differentiated tissues.
The local biosynthesis of the phytohormone auxin and its directional intercellular transport are essential in these processes because they provide positional information and link cell polarity with tissue patterning 1 — 3.
PIN proteins are cellular auxin export carriers and their polar subcellular localization at the plasma membrane determines the direction of the intercellular auxin flow 4 , 5. PIN proteins undergo constitutive endocytic recycling between the plasma membrane and the endosomal compartments 6 , 7 , but the functional role of this recycling mechanism is still unclear.
A plausible assumption is that constitutive trafficking regulates the cellular auxin transport rates 6 and accounts for the flexibility needed for the rapid PIN polarity changes that allow the auxin flow to be quickly redirected in response to various signals, including environmental or developmental cues 8 — Indeed, dynamic PIN translocation between different cell sides termed transcytosis can be pharmacologically induced in plant cells and might account for rapid PIN alterations during plant development 9 , Rapid changes in PIN polarities occur during embryonic development 11 , aerial and underground organogenesis 12 — 15 , vascular tissue formation 16 , and root gravity responses 17 , However, the underlying mechanism of these PIN polarity alterations still needs to be demonstrated.
The developmentally regulated changes in PIN polarity presumably redirect auxin fluxes and, subsequently, trigger alterations in the developmental programs 19 — An intriguing example of PIN polarity reorganization relates to the perception and response to environmental stimuli. For example, when the root is reoriented in a horizontal position, gravity-sensing statoliths in the columella cells sediment toward the new bottom side of these cells and PIN3 relocalizes from its originally uniform distribution to this side 17 , 18 , The asymmetric repositioning of PIN3 is presumably followed by a downward auxin flow, leading to auxin accumulation at the bottom side of the root and, consequently, to asymmetric tissue growth and downward root bending Despite the fundamental importance of PIN-dependent auxin transport for plant gravitropic responses, the underlying mechanism for PIN3 polarization remains to be established.
Here, we examined the cellular and molecular mechanism for PIN3 polarization in response to gravity. Moreover, live imaging reveals endosome-based translocation of PIN3 proteins between different cell sides. Our data suggest that gravity modulates multiple steps of PIN3 trafficking leading to PIN3 transcytosis that has presumably physiological importance for the redirection of auxin fluxes during gravitropic response. Despite the anticipated importance of PIN3 for root gravitropism and its demonstrated role in shoot gravitropism, pin3 mutant roots are only marginally defective in responding to gravity 17 Fig.
In accordance with this assumption, we found that PIN3 and its closest homolog, PIN7, display partially overlapping expression patterns in columella cells. S1B , indicating a PIN7-dependent compensation of auxin flux in pin3 mutant columella cells. Consistently, the gravitropic response defects of the pin3 pin7 double-mutant seedlings were stronger than those of either single mutant Fig. Other PIN proteins, such as PIN4, which are also produced in the root tip 28 , might contribute to gravity-induced auxin redistribution.
However, higher order pin mutants, such as pin3 pin4 pin7, display strong developmental defects 25 , 26 ; hence, their contribution to the gravitropic response is difficult to assess. Nevertheless, our findings show that PIN auxin transporters act redundantly in gravity-sensing columella cells during the gravity response.
Differential growth during tropisms mainly involves changes in cell expansion versus changes in cell division, although a role for cell division in tropic growth has not been formally ruled out. Gravity is sensed in the root tip and this information must then be relayed to the elongation zone so as to maintain growth direction and mount effective growth responses to changes in orientation to and continue to grow its roots in the same direction as gravity. The model was independently proposed by the Russian scientist N. Cholodny of the University of Kiev in and by Frits Went of the California Institute of Technology in , both based on work they had done in This behavior is described as a "tipping point" mechanism for auxin transport in response to a gravitational stimulus. This suppresses growth on this side, while allowing cell elongation on the top of the root.
Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells
Tropism Abstract Gravity perception plays a key role in how plants develop and adapt to environmental changes. However, more than a century after the pioneering work of Darwin, little is known on the sensing mechanism. Using a centrifugal device combined with growth kinematics imaging, we show that shoot gravitropic responses to steady levels of gravity in four representative angiosperm species is independent of gravity intensity. All gravitropic responses tested are dependent only on the angle of inclination from the direction of gravity. We thus demonstrate that shoot gravitropism is stimulated by sensing inclination not gravitational force or acceleration as previously believed. This contrasts with the otolith system in the internal ear of vertebrates and explains the robustness of the control of growth direction by plants despite perturbations like wind shaking. Our results will help retarget the search for the molecular mechanism linking shifting statoliths to signal transduction.
Gravity sensing, a largely misunderstood trigger of plant orientated growth
Search Menu Abstract Plant organs control their growth orientation in response to gravity. Within gravity-sensing cells, the input gravity sensing and signal conversion gravity signalling progress sequentially. The cells contain a number of high-density, starch-accumulating amyloplasts, which sense gravity when they reposition themselves by sedimentation to the bottom of the cell when the plant organ is re-orientated. This triggers the next step of gravity signalling, when the physical signal generated by the sedimentation of the amyloplasts is converted into a biochemical signal, which redirects auxin transport towards the lower flank of the plant organ. This review focuses on recent advances in our knowledge of the regulatory mechanisms that underlie amyloplast sedimentation and the system by which this is perceived, and on recent progress in characterising the factors that play significant roles in gravity signalling by which the sedimentation is linked to the regulation of directional auxin transport.