Defining the Site of Light Perception and Initiation of Phototropism in Arabidopsis

Preuten, Tobias; Hohm, Tim; Bergmann, Sven; Fankhauser, Christian

doi:10.1016/j.cub.2013.07.079

Cited by 45 publications

(75 citation statements)

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“…5). Very recently, it has been reported that the upper parts of Arabidopsis shoots are very important for the perception of phototropic signals and in the production of auxin asymmetrical distribution (Preuten et al, 2013;Yamamoto et al, 2014). Furthermore, severe impairment of phototropic responses in the phot1 mutant was complemented by the expression of phot1 in epidermal cells (Preuten et al, 2013).…”

Section: Discussionmentioning

confidence: 88%

“…Careful analysis with the pid single mutant showed that PID is partially involved in both the pulse-induced first positive phototropism and the time-dependent second positive phototropism . Furthermore, the pid wag1 wag2 triple mutant showed partial impairment of the continuous light-induced second positive phototropism (Ding et al, 2011;Preuten et al, 2013). Therefore, the PID family seemed to be one of the key components for the regulation of phototropic responses.…”

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confidence: 99%

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PINOID AGC Kinases Are Necessary for Phytochrome-Mediated Enhancement of Hypocotyl Phototropism in Arabidopsis

2014

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Several members of the AGCVIII kinase subfamily, which includes PINOID (PID), PID2, and WAVY ROOT GROWTH (WAG) proteins, have previously been shown to phosphorylate PIN-FORMED (PIN) auxin transporters and control the auxin flow in plants. PID has been proposed as a key component of the phototropin signaling pathway that induces phototropic responses, although the responses were not significantly impaired in the pid single and pid wag1 wag2 triple mutants. This raises questions about the functional roles of the PID family in phototropic responses. Here, we investigated hypocotyl phototropism in the pid pid2 wag1 wag2 quadruple mutant in detail to clarify the roles of the PID family in Arabidopsis (Arabidopsis thaliana). The pid quadruple mutants exhibited moderate responses in continuous light-induced phototropism with a decrease in growth rates of hypocotyls and normal responses in pulse-induced phototropism. However, they showed serious defects in enhancements of pulse-induced phototropic curvatures and lateral fluorescent auxin transport by red light pretreatment. Red light pretreatment significantly reduced the expression level of PID, and the constitutive expression of PID prevented pulse-induced phototropism, irrespective of red light pretreatment. This suggests that the PID family plays a significant role in phytochrome-mediated phototropic enhancement but not the phototropin signaling pathway. Red light treatment enhanced the intracellular accumulation of PIN proteins in response to the vesicle-trafficking inhibitor brefeldin A in addition to increasing their expression levels. Taken together, these results suggest that red light preirradiation enhances phototropic curvatures by upregulation of PIN proteins, which are not being phosphorylated by the PID family.Sessile organisms, such as plants, develop many adaptational mechanisms. Phototropism is one such acclimation response in plants to light environments, by which they can advantageously obtain light energy for photosynthesis. So far, phototropic responses, which have been well studied for many years, are separated mainly into two types according to their characters: the first positive phototropism and the second positive phototropism (Iino, 2001;Whippo and Hangarter, 2006;Briggs, 2014). The first positive phototropism is induced by a pulse of blue light, and the magnitudes of the responses are dependent totally on the total light fluence. However, the second positive phototropism is induced by a prolonged irradiation of blue light, and the extent of the curvature responses depends on the duration of the blue light illumination and not on the total light fluences.Classical physiological analysis has revealed that plant photoreceptor phytochromes influence phototropin (phot)-mediated phototropic responses in several aspects (Iino, 2001;Whippo and Hangarter, 2006;Sakai and Haga, 2012;Briggs, 2014). For the first positive pulse-induced phototropism, phytochromes are involved in the enhancement of phototropic curvatures in addition to desensitization (Liu...

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Section: Discussionmentioning

confidence: 88%

mentioning

confidence: 99%

PINOID AGC Kinases Are Necessary for Phytochrome-Mediated Enhancement of Hypocotyl Phototropism in Arabidopsis

2014

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“…Initiation of lateral auxin gradients has been observed in the upper hypocotyl of de‐etiolated seedlings (Christie et al ., ), implying that this region is important for light perception. Decapitation experiments concur with this conclusion as curvature is still observed when the cotyledons are excised (Christie et al ., ), but is reduced when the cotyledonary node, including the shoot apical meristem (SAM) and leaf primordia are removed (Preuten et al ., ). Similar decapitation experiments have been performed using etiolated seedlings and again localize the site of light perception to the upper hypocotyl (Preuten et al ., ; Yamamoto et al ., ).…”

Section: Introductionmentioning

confidence: 97%

“…Traditionally, dark‐grown (etiolated) seedlings are used to study phototropism in both monocotyledonous and dicotyledonous species (Christie and Murphy, ). Recent studies using the model flowering plant, Arabidopsis thaliana have extended this analysis to light‐grown (de‐etiolated) seedlings which show retained phototropic responsiveness (Christie et al ., ; Preuten et al ., , ) Yet, despite over a decade of research, the signalling mechanisms underlying this differential growth response remain largely unresolved.…”

Section: Introductionmentioning

confidence: 99%

Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex

et al. 2016

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SummaryPhototropin (phot1) is a blue light‐activated plasma membrane‐associated kinase that acts as the principal photoreceptor for shoot phototropism in Arabidopsis in conjunction with the signalling component Non‐Phototropic Hypocotyl 3 (NPH3). PHOT1 is uniformly expressed throughout the Arabidopsis hypocotyl, yet decapitation experiments have localized the site of light perception to the upper hypocotyl. This prompted us to investigate in more detail the functional role of the hypocotyl apex, and the regions surrounding it, in establishing phototropism. We used a non‐invasive approach where PHOT1–GFP (P1–GFP) expression was targeted to the hypocotyl apex of the phot‐deficient mutant using the promoters of CUP‐SHAPED COTYLEDON 3 (CUC3) and AINTEGUMENTA (ANT). Expression of CUC3::P1–GFP was clearly visible at the hypocotyl apex, with weaker expression in the cotyledons, whereas ANT::P1–GFP was specifically targeted to the developing leaves. Both lines showed impaired curvature to 0.005 μmol m−2 sec−1 unilateral blue light, indicating that regions below the apical meristem are necessary for phototropism. Curvature was however apparent at higher fluence rates. Moreover, CUC3::P1–GFP partially or fully complemented petiole positioning, leaf flattening and chloroplast accumulation, but not stomatal opening. Yet, tissue analysis of NPH3 de‐phosphorylation showed that CUC3::P1–GFP and ANT::P1–GFP mis‐express very low levels of phot1 that likely account for this responsiveness. Our spatial targeting approach therefore excludes the hypocotyl apex as the site for light perception for phototropism and shows that phot1‐mediated NPH3 de‐phosphorylation is tissue autonomous and occurs more prominently in the basal hypocotyl.

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“…While PIN3 relocalization may not be the major contributor to phototropism, PIN3 phosphorylation appears to be. PIN3 appears to contribute primarily in auxin movement to the hypocotyl elongation zone after lateral auxin redistribution takes place (Christie et al 2011, Preuten et al 2013. D6PK is a protein kinase that activates the transport activity of PIN proteins (Zourelidou et al 2009, Willige et al 2013.…”

Section: Altered Pin Function Is Not Always a Results Of Altered Pin Pmentioning

confidence: 99%

Measure for measure: determining, inferring and guessing auxin gradients at the root tip

Peer

Jenness

Murphy

2014

Physiologia Plantarum

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The plant hormone auxin is transported from sites of synthesis to sites of action. Auxin responses are mediated by fast (non-transcriptional) and slow (transcriptional; ubiquitinylation) responses, which affect physiological changes at cellular and organismal scales. As such, auxin transport vectors regulate programmed and plastic growth responses to optimize growth and development. Here we address some common problems in extrapolating 'universal' understanding of auxin transport streams from analyses of loss-of-function mutants and auxin transport inhibitors. We also discuss the analytical methods and tools used to directly quantify, measure and infer auxin gradients within the plant [DR5:GUS/GFP (beta-glucuronidase/green fluorescent protein), DII-VENUS; surface electrodes, direct quantification]. We discuss the assumptions and limitations of each of these analyses, present comparative summaries of auxin transport methods and assay conditions (diffusion, non-specific transport and relevant assay conditions), and consider what is actually being transported and measured [labeled-indole-3-acetic acid (IAA), IAA metabolites].

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Defining the Site of Light Perception and Initiation of Phototropism in Arabidopsis

Cited by 45 publications

References 51 publications

PINOID AGC Kinases Are Necessary for Phytochrome-Mediated Enhancement of Hypocotyl Phototropism in Arabidopsis

PINOID AGC Kinases Are Necessary for Phytochrome-Mediated Enhancement of Hypocotyl Phototropism in Arabidopsis

Functional characterization of Arabidopsis phototropin 1 in the hypocotyl apex

Measure for measure: determining, inferring and guessing auxin gradients at the root tip

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