A phosphorylation switch turns a positive regulator of phototropism into an inhibitor of the process

Schumacher, Paolo; Demarsy, Emilie; Waridel, Patrice; Petrolati, Laure Allenbach; Trevisan, Martine; Fankhauser, Christian

doi:10.1038/s41467-018-04752-1

Cited by 28 publications

(34 citation statements)

References 47 publications

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“…Recent work has shown that PKS4 acts in conjunction with phot1 to reduce phototropic responsiveness at higher light intensities (Schumacher et al, 2018). PKS4 is phosphorylated by phot1 (Demarsy et al, 2012), and the accumulation of its phosphorylated form has been shown to delay phototropism (Schumacher et al, 2018). However, this occurs by a mechanism that does not affect NPH3 dephosphorylation (Schumacher et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

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Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Sullivan

Kharshiing²,

Laird

et al. 2019

Plant Physiol.

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Phototropin (phot) receptor kinases play important roles in promoting plant growth by controlling light-capturing processes, such as phototropism. Phototropism is mediated through the action of NON-PHOTOTROPIC HYPOCOTYL3 (NPH3), which is dephosphorylated following phot activation. However, the functional significance of this early signaling event remains unclear. Here, we show that the onset of phototropism in dark-grown (etiolated) seedlings of Arabidopsis (Arabidopsis thaliana) and tomato (Solanum lycopersicum) is enhanced by greening (deetiolation). Red and blue light were equally effective in promoting phototropism in Arabidopsis, consistent with our observations that deetiolation by phytochrome or cryptochrome was sufficient to enhance phototropism. Increased responsiveness did not result from an enhanced sensitivity to the phytohormone auxin, nor does it involve the phot-interacting protein, ROOT PHOTOTROPISM2. Instead, deetiolated seedlings showed attenuated levels of NPH3 dephosphorylation and diminished relocalization of NPH3 from the plasma membrane during phototropism. Likewise, etiolated seedlings that lack the PHYTOCHROME-INTERACTING FACTORS (PIFs) PIF1, PIF3, PIF4, and PIF5 displayed reduced NPH3 dephosphorylation and enhanced phototropism, consistent with their constitutive photomorphogenic phenotype in darkness. Phototropic enhancement could also be achieved in etiolated seedlings by lowering the light intensity to diminish NPH3 dephosphorylation. Thus, phototropism is enhanced following deetiolation through the modulation of a phosphorylation rheostat, which in turn sustains the activity of NPH3. We propose that this dynamic mode of regulation enables young seedlings to maximize their establishment under changing light conditions, depending on their photoautotrophic capacity.

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Section: Discussionmentioning

confidence: 99%

“…PKS4 is phosphorylated by phot1 (Demarsy et al, 2012), and the accumulation of its phosphorylated form has been shown to delay phototropism (Schumacher et al, 2018). However, this occurs by a mechanism that does not affect NPH3 dephosphorylation (Schumacher et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Sullivan

Kharshiing²,

Laird

et al. 2019

Plant Physiol.

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show abstract

“…Unlike etiolated seedlings, which show high sensitivity to directional blue light, de-etiolated seedlings growing in full sunlight do not show a strong phototropic response (Goyal et al, 2016;Schumacher et al, 2018). However, LRFR, which is typical of shaded environments, enhances phototropism (Ballaré et al, 1992;Goyal et al, 2016).…”

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confidence: 99%

Low Blue Light Enhances Phototropism by Releasing Cryptochrome1-Mediated Inhibition of PIF4 Expression

et al. 2020

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“…Unlike etiolated seedlings, which show high sensitivity to directional blue light, de-etiolated seedlings growing in full sunlight do not show a strong phototropic response (Goyal et al, 2016; Schumacher et al, 2018). However, LRFR, which is typical of shaded environments, enhances phototropism (Ballare et al, 1992; Goyal et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

In Arabidopsis, low blue light enhances phototropism by releasing cryptochrome 1-mediated inhibition ofPIF4expression

Boccaccini

Legris

Krahmer

et al. 2020

Preprint

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Shade-avoiding plants including Arabidopsis thaliana display a number of growth responses elicited by shade cues including elongation of stem-like structures and repositioning of leaves. Shade also promotes phototropism of de-etiolated seedlings through repression of phytochrome B (phyB) presumably to enhance capture of unfiltered sunlight. Light cues indicative of shade include a reduction in the blue and red portions of the solar spectrum and a low red to far-red ratio. Here we show that in Arabidopsis seedlings both low blue and a low red to far-red ratio are required to rapidly enhance phototropism. However, prolonged low blue treatments through reduced cryptochrome 1 (cry1) activation are sufficient to promote phototropism. The enhanced phototropic response of cry1 mutants in the lab and in response to natural canopies depends on PHYTOCHROME INTERACTING FACTORs (PIFs). In favorable light conditions, cry1 limits the expression of PIF4 while in low blue light PIF4 expression increases, which contributes to phototropic enhancement. The analysis of a quantitative DII auxin reporter indicates that low blue light leads to enhanced auxin levels in the hypocotyl and, upon phototropic stimulation, a steeper auxin gradient across the hypocotyl. We conclude that phototropic enhancement by canopy shade results from the combined activities of phytochrome B and cry1 that converge on PIF regulation.ONE SENTENCE SUMMARYThe persistent depletion of blue light in natural canopy shade relieves the inhibitory effect of cryptochrome 1 on PIF4, enhancing phototropism in de-etiolated Arabidopsis seedlings.Financial supportThis work was supported by the University of Lausanne and a grant from the Swiss National Science foundation (n° 310030B_179558 to C.F.); Human Frontier Science Program organization (HFSP) Grant RPG0054-2013, ANR-12-BSV6-0005 grant (AuxiFlo) to T.V.; The University of Buenos Aires (Grant 20020100100437 to J. J. C.), and Agencia Nacional de Promoción Científica y Tecnológica of Argentina (Grant PICT-2018-01695 to J. J. C.). Alessandra Boccaccini and Martina Legris are funded by Marie Curie fellowships H2020-MSCA-IF-2017 grants CRoSh 796283 and Flat-Leaf 796443 respectively.

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A phosphorylation switch turns a positive regulator of phototropism into an inhibitor of the process

Cited by 28 publications

References 47 publications

Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Deetiolation Enhances Phototropism by Modulating NON-PHOTOTROPIC HYPOCOTYL3 Phosphorylation Status

Low Blue Light Enhances Phototropism by Releasing Cryptochrome1-Mediated Inhibition of PIF4 Expression

In Arabidopsis, low blue light enhances phototropism by releasing cryptochrome 1-mediated inhibition ofPIF4expression

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