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. 2014 Jan;26(1):38-55.
doi: 10.1105/tpc.113.119727. Epub 2014 Jan 30.

Phototropism: growing towards an understanding of plant movement

Emmanuel Liscum  1 , Scott K Askinosie, Daniel L Leuchtman, Johanna Morrow, Kyle T Willenburg, Diana Roberts Coats
Affiliations

Phototropism: growing towards an understanding of plant movement

Emmanuel Liscum et al. Plant Cell. 2014 Jan.

Abstract

Phototropism, or the differential cell elongation exhibited by a plant organ in response to directional blue light, provides the plant with a means to optimize photosynthetic light capture in the aerial portion and water and nutrient acquisition in the roots. Tremendous advances have been made in our understanding of the molecular, biochemical, and cellular bases of phototropism in recent years. Six photoreceptors and their associated signaling pathways have been linked to phototropic responses under various conditions. Primary detection of directional light occurs at the plasma membrane, whereas secondary modulatory photoreception occurs in the cytoplasm and nucleus. Intracellular responses to light cues are processed to regulate cell-to-cell movement of auxin to allow establishment of a trans-organ gradient of the hormone. Photosignaling also impinges on the transcriptional regulation response established as a result of changes in local auxin concentrations. Three additional phytohormone signaling pathways have also been shown to influence phototropic responsiveness, and these pathways are influenced by the photoreceptor signaling as well. Here, we will discuss this complex dance of intra- and intercellular responses that are regulated by these many systems to give rise to a rapid and robust adaptation response observed as organ bending.

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Figures

Figure 1.
Figure 1.
BL-Induced Phototropism in Higher Plants Requires the Establishment of a Differential Gradient of Auxin. (A) Diagram of a hypocotyl exhibiting a phototropic response. Auxin synthesized in the apical portions of the stem is polarly transported toward the root predominately through the central vasculature and to a lesser extent via epidermal and subepidermal cell layers (downward pointing red arrows). While in dark-grown seedlings the amount of auxin transported through the outer cell layers is not appreciably different side-to-side across the hypocotyl (data not shown), in seedlings exposed to directional BL, a differential of downward auxin flow is established (see downward pointing outer red arrows). Directional BL also induces a lateral redistribution of auxin from the lit to shaded portion of the hypocotyl (trans-hypocotyl red arrows). Together, these actions result in the differential accumulation of auxin in the elongation zone of shaded versus lit sides of the seedling (yellow shading). (B) Cross section within the elongation zone of an Arabidopsis seedling hypocotyl illustrating the gradients of phot1 activity (false-colored white to blue) and auxin accumulation (false-colored white to yellow). Gray dots are meant to represent nuclei within the outer two cell layers, regions particularly important to auxin-mediated transcriptional responses (see Figures 3 and 4). Cells outlined in green are endodermal cells.
Figure 2.
Figure 2.
Early Phototropic Signaling Events Involved in the Regulation of Auxin Transport That Leads to a Differential Gradient of the Hormone. (A) Hypocotyl cell in darkness. Auxin is moving from the cell wall space to the cytoplasm across the plasma membrane (thick black line) either passively (as IAAH) or via AUX/LAX (purple)–mediated H+-cotransport (as IAA−). Anionic auxin within the cytoplasm can only leave the cell via PIN (light orange) or ABCB (yellow) facilitator–mediated transport. PIN proteins are polarly localized more to basal ends of cells in dark-grown seedlings (thus providing for bulk polar downward flow of auxin depicted in Figure 1), though they also exhibit cycling between the plasma membrane and endosomes through a mechanism regulated by ARF-GEFs and AGC3 kinases (boxed in purple). PIN protein stability at the plasma membrane is enhanced by the presence of ABCB19 (reflected by the gray repression on endocytotic events). By contrast, free ABP not bound to auxin (brown) on the outer surface of the plasma membrane promotes endocytosis of PIN proteins. phot1 (red) is in its dephosphorylated inactive state, as is the Cullin 3-RBX-E3 (CRL) complex (blue-violet). phot1 is shown as its two functional domains; the light-sensing FMN (black stars) binding half, attached to the output PKD via the Jα-helix (black). NPH3 (light green) is present in its phosphorylated inactive state. phot1, NPH3, PKS (dark orange), and ABCB19 are part of a protein complex at the plasma membrane. Auxin is fairly evenly distributed around and within the cell as represented by the consistent light-yellow shading. (B) Hypocotyl cell after exposure to directional BL (from the right). phot1 (dark green with white stars) is in its active state, promoting phosphorylation (black balls with “P”) of ABCB19, PKS, and phot1 itself. Activation of phot1 also promotes the dephosphorylation of NPH3 (light green) by a presently unidentified type 1 protein phosphatase (data not shown). The CRL complex interacts (light blue) with NPH3 upon photoactivation of phot1, resulting in the ubiquitination (red ball with “U”) of phot1. Phosphorylation (and possibly mono/multiubiquitination) of phot1 further promotes the movement of phot1 away from the plasma membrane. Phosphorylation of ABCB19 suppresses its transport activity and appears to disrupt the stabilizing effect of ABCB19 on PIN protein localization to the plasma membrane. phot1 activation also stimulates the relocalization of PIN proteins to the lateral face of cell, a process that is potentially enhanced by auxin-bound ABP at the cell surface, which can repress endocytosis of PIN proteins. All of these effects lead to a redistribution of auxin from a polar basal flow to a lateral flow away from the light source (graded yellow background).
Figure 3.
Figure 3.
Model for Regulation of Transcription by Auxin. (A) A nucleus of a hypocotyl cell in a dark-grown seedling with only basal levels of auxin present. ARF transcription factors, such as NPH4/ARF7 (red), are bound to DNA target sequences (AuxRE) within the nuclear DNA as heteromeric complexes with a dominant transcriptional repressor protein, such as AUX/IAA19 (gold) and a corepressor, such as TPL (orange). This complex is transcriptionally inactive, and, as such, transcription of auxin-regulated genes is repressed (red X). Also present in the nucleus is the SCFTIR1/AFB auxin receptor complex (blue-violet and light green) in its inactive ligand (auxin)-free state. (B) A nucleus of a hypocotyl cell that is in the shaded portion of a seedling exposed to directional BL where auxin has accumulated. Elevated auxin levels stimulate the binding of AUX/IAA proteins, such as IAA19, to the SCFTIR1/AFB complex (green and light blue), which in turn promotes the polyubiquitination of the AUX/IAA protein and its subsequent degradation by a 26S proteasome (gray). Removal of AUX/IAA proteins releases the corepressor TPL and allows for homodimerization of ARF proteins, which stimulates RNA polymerase core protein activation and transcription of target genes, such as TSI genes.
Figure 4.
Figure 4.
A Cellular Model for Auxin-Mediated Differential Cell Elongation in Phototropically Stimulated Hypocotyls. Initial photosensory events in phototropism result in a redistribution of auxin (yellow shading) such that it accumulates in the cells within the elongation zone of the hypocotyl farthest from the incident light (see Figures 1 and 2). Differential accumulation of auxin leads to the homodimerization and activation of NPH4/ARF7 (red and green nuclear proteins) in a graded fashion across the hypocotyl through auxin-mediated degradation of the IAA19 (gold) repressor protein and release of the corepressor TPL (orange) (see Figure 3). This differential in ARF activity thus results in the expression of tropic stimulus-induced genes, such as EXPANSINs (EXP), in the cells where auxin levels have increased beyond a threshold necessary to stimulate AUX/IAA degradation. EXP mRNAs (blue) are then translated into EXP protein, which is then deposited in the cell wall such that EXP protein accumulates beyond its basal level found in unstimulated seedlings (e.g., like that observed in the lit flank; red EXP ball) in regions farthest from the incident light stimulation. Increased auxin levels also stimulate (again in a graded fashion across the hypocotyl) a plasma membrane–localized H+-ATPase (purple) that pumps H+ out of the cell such that the extracellular matrix is acidified, a process that in turn activates the enzymatic activity of the EXP proteins in the wall to promote cell elongation.
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References

    1. Abas L., Benjamins R., Malenica N., Paciorek T., Wiśniewska J., Moulinier-Anzola J.C., Sieberer T., Friml J., Luschnig C. (2006). Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8: 249–256 Erratum. Nat. Cell Biol. 8: 424. - PubMed
    1. Aihara Y., Tabata R., Suzuki T., Shimazaki K., Nagatani A. (2008). Molecular basis of the functional specificities of phototropin 1 and 2. Plant J. 56: 364–375 - PubMed
    1. Ambrose C., Ruan Y., Gardiner J., Tamblyn L.M., Catching A., Kirik V., Marc J., Overall R., Wasteneys G.O. (2013). CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev. Cell 24: 649–659 - PubMed
    1. Bennett M.J., Marchant A., Green H.G., May S.T., Ward S.P., Millner P.A., Walker A.R., Schulz B., Feldmann K.A. (1996). Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273: 948–950 - PubMed
    1. Blakeslee J.J., et al. (2007). Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19: 131–147 - PMC - PubMed

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