Shining Light on the Function of NPH3/RPT2-Like Proteins in Phototropin Signaling
Open accessAbstract
Plasma membrane receptors play fundamental roles in shaping plant growth and development. A large proportion of these are autophosphorylating Ser/Thr kinases (De Smet et al., 2009). Some function as dual-specificity kinases, autophosphorylating additionally on Tyr residues, one of which is the extensively studied steroid receptor BRASSINOSTEROID-INSENSITIVE1 (BRI1; Oh et al., 2009). Light regulation of plant growth also is mediated by plasma membrane-bound Ser/Thr kinases known as the phototropins (phots; Fankhauser and Christie, 2015). Seed plants contain two phots (phot1 and phot2) that have important roles in regulating leaf positioning and expansion, chloroplast photorelocation movement, stomatal opening, and phototropism, all of which serve to optimize photosynthetic efficiency (Christie et al., 2015). Phots are members of the AGCVIII kinase family (Rademacher and Offringa, 2012) but are distinct from transmembrane receptor kinases such as BRI1, as they are hydrophilic and bind to the intracellular side of the plasma membrane (Kong et al., 2013) to initiate signaling (Preuten et al., 2015). Although the ability to associate with the plasma membrane is conserved in algal phots (Sullivan et al., 2016a), the mechanism underlying this attachment is still not known, but it is thought to involve some form of lipid binding/modification. Kinase-inactive versions of phot1 and phot2 are nonfunctional, highlighting the importance of receptor autophosphorylation in phot signaling (Inoue et al., 2008a, 2011). Autophosphorylation occurs predominantly on multiple Ser residues. At least 21 and 29 phosphorylation sites have been identified for Arabidopsis (Arabidopsis thaliana) phot1 and phot2, respectively (Christie et al., 2015). Most of these sites are found in the N terminus of the protein, which contains two light-sensing modules known as LIGHT, OXYGEN, OR VOLTAGE SENSING (LOV) domains known as LOV1 and LOV2 (Christie et al., 2012). Autophosphorylation of Ser-350, Ser-376, and Ser-410 within the LOV-linker region promotes the binding of 14-3-3 regulatory proteins to phot1 (Inoue et al., 2008a; Sullivan et al., 2009). However, the biological significance of this interaction is still not known. The occurrence of some these phosphorylation sites also is fluence rate dependent (Salomon et al., 2003) and is thought to play a role in receptor desensitization (Christie and Murphy, 2013). By contrast, the autophosphorylation of two conserved Ser residues within the activation loop of the C-terminal kinase domain (Ser-849 and Ser-851 in phot1 and Ser-761 or Ser-763 in phot2) is necessary for receptor signaling (Inoue et al., 2008a, 2011). Mutation of these sites to Ala impairs phot1 function in Arabidopsis, whereas phosphomimetic substitutions to Asp are without effect (Inoue et al., 2008a). Despite considerable efforts over the last two decades, the signaling events that follow receptor autophosphorylation remain poorly understood for most phot-mediated responses. Yet, it is becoming increasingly apparent that members of the NPH3/RPT2-Like family (NRL) are required to elicit several phot responses. Moreover, accumulating evidence suggests that these plant-specific proteins act in concert with different AGCVIII kinases to regulate various aspects of auxin transport and signaling. In this review, we summarize our current understanding of the biochemical properties of the NRL family in Arabidopsis and how these proteins function to coordinate different aspects of phot signaling. We also discuss to what extent these signaling processes are conserved in land plants and algae. The NRL family is named after its two founding members, NONPHOTOTROPIC HYPOCOTYL3 (NPH3) and ROOT PHOTOTROPISM2 (RPT2; Liscum et al., 2014), which were first identified from genetic screens for Arabidopsis mutants impaired in hypocotyl and root phototropism (Okada and Shimura, 1992; Liscum and Briggs, 1995; Sakai et al., 2000). The primary amino acid structure of NRL proteins can be separated into three main parts based on sequence conservation: a BTB (bric-a-brac, tramtrack, and broad complex) domain at the N terminus, followed by an NPH3 domain and a C-terminal coiled-coil domain (Liscum et al., 2014). In addition to NPH3 and RPT2, Arabidopsis contains another 31 NPH3/RPT2-Like proteins (NRL1–NRL31), all of which are defined by the presence of the NPH3 domain (Pedmale et al., 2010). Ten of these members lack the C-terminal coiled-coli domain, whereas two are devoid of the BTB domain (Pedmale et al., 2010). The reasons for these differences in domain structure are not clear at present, because many of these NRL proteins have yet to be ascribed a biological function. Functions for 10 out of the 33 Arabidopsis NRL proteins have been identified so far. Phylogenetic analysis has shown that NRL proteins can be classified into seven distinct clades in land plants (Suetsugu et al., 2016). However, in angiosperms such as Arabidopsis, only six of these clades are
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- Authors
- Christie, J. M., Suetsugu, N., Sullivan, S., & Wada, M.
- Affiliations
- University of Glasgow (GB)
- Kyoto University (JP)
- Tokyo Metropolitan University (JP)
- Venue
- Plant Physiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2017-07-18
- Volume
- 176
- Issue
- 2
- Pages
- 1015-1024
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC5813532
- OpenAlex
- W2738907217
- Cited by
- 81
- References
- 81
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 12 · 2023: 7 · 2022: 9 · 2021: 15 · 2020: 7 · 2019: 7 · 2018: 4
- FWCI
- 0.51
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- PLANT PHYSIOLOGY (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- ENLIGHTEN (Jurnal Bimbingan dan Konseling Islam) (acceptedVersion, cc-by-sa)
- Funders
- Biotechnology and Biological Sciences Research Council (BB/M002128/1)
- Japan Society for the Promotion of Science (16K14758)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Keywords
- phototropin, receptor autophosphorylation, LOV domain, phot1, phot2, Arabidopsis thaliana, light signaling, phototropism, leaf expansion, stomatal opening
- MeSH terms
- Light, Phosphoproteins, Phylogeny, Phytochrome, Signal Transduction, Protein Serine-Threonine Kinases, Arabidopsis, Gene Expression Regulation, Plant, Phototropism, Arabidopsis Proteins
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