Arabidopsis ROOT PHOTOTROPISM2 Contributes to the Adaptation to High-Intensity Light in Phototropic Responses

Abstract

Living organisms adapt to changing light environments via mechanisms that enhance photosensitivity under darkness and attenuate photosensitivity under bright light conditions. In hypocotyl phototropism, phototropin1 (phot1) blue light photoreceptors mediate both the pulse light-induced, first positive phototropism and the continuous light-induced, second positive phototropism, suggesting the existence of a mechanism that alters their photosensitivity. Here, we show that light induction of ROOT PHOTOTROPISM2 (RPT2) underlies photosensory adaptation in hypocotyl phototropism of Arabidopsis thaliana. rpt2 loss-offunction mutants exhibited increased photosensitivity to very low fluence blue light but were insensitive to low fluence blue light. Expression of RPT2 prior to phototropic stimulation in etiolated seedlings reduced photosensitivity during first positive phototropism and accelerated second positive phototropism. Our microscopy and biochemical analyses indicated that blue light irradiation causes dephosphorylation of NONPHOTOTROPIC HYPOCOTYL3 (NPH3) proteins and mediates their release from the plasma membrane. These phenomena correlate closely with the desensitization of phot1 signaling during the transition period from first positive phototropism to second positive phototropism. RPT2 modulated the phosphorylation of NPH3 and promoted reconstruction of the phot1-NPH3 complex on the plasma membrane. We conclude that photosensitivity is increased in the absence of RPT2 and that this results in the desensitization of phot1. Light-mediated induction of RPT2 then reduces the photosensitivity of phot1, which is required for second positive phototropism under bright light conditions.

Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling

“…A detailed discussion of phototropism is beyond the scope of this review, and readers are directed to other articles that provide a comprehensive overview of the different types of photophysiological responses involved (Sakai and Haga, 2012;Christie and Murphy, 2013). While the biochemical function of NPH3 remains poorly understood, it appears to be instrumental for establishing lateral auxin gradients required for this differential growth response (Haga et al, 2015). NPH3 is localized to the plasma membrane and has been shown to interact directly with phot1 via its C-terminal region (Motchoulski and Liscum, 1999).…”

“…A recent in vivo coimmunoprecipitation analysis indicates that phot1-NPH3 interactions at the plasma membrane are transiently disrupted upon irradiation (Haga et al, 2015). Light not only impacts the ability of NPH3 to interact with phot1 but also leads to dynamic changes in its subcellular localization.…”

“…Light not only impacts the ability of NPH3 to interact with phot1 but also leads to dynamic changes in its subcellular localization. The expression of YFP-NPH3 under the control of the constitutive cauliflower mosaic virus 35S promoter restores hypocotyl phototropism in the nph3 mutant (Haga et al, 2015). YFP-NPH3 is localized to the plasma membrane in darkness but is rapidly (within minutes) internalized into microdomain aggregates upon phot1 activation by blue light (Haga et al, 2015).…”

“…The expression of YFP-NPH3 under the control of the constitutive cauliflower mosaic virus 35S promoter restores hypocotyl phototropism in the nph3 mutant (Haga et al, 2015). YFP-NPH3 is localized to the plasma membrane in darkness but is rapidly (within minutes) internalized into microdomain aggregates upon phot1 activation by blue light (Haga et al, 2015). The appearance of these microdomains is diminished in periods of prolonged irradiation or when seedlings are returned to darkness, suggesting that their formation is reversible (Haga et al, 2015).…”

“…YFP-NPH3 is localized to the plasma membrane in darkness but is rapidly (within minutes) internalized into microdomain aggregates upon phot1 activation by blue light (Haga et al, 2015). The appearance of these microdomains is diminished in periods of prolonged irradiation or when seedlings are returned to darkness, suggesting that their formation is reversible (Haga et al, 2015). The biological significance and the role of these microdomains in phot signaling are currently unknown.…”