The Phototropin Family of Photoreceptors

Abstract

The past decade has seen dramatic advances in our knowledge of plant photoreceptors and in our understanding of the signal transduction pathways that they activate (Briggs and Olney, 2001). A major part of these advances has been the identification and characterization of photoreceptors that respond to signals from the blue region of the electromagnetic spectrum. We now know that there are at least two classes of blue light photoreceptors: the cryptochromes and the phototropins. The purpose of this letter is to establish a uniform terminology for the phototropins. Knowledge of their occurrence across the plant kingdom, their structure, and their unique photochemistry is growing at a rapid rate, and it is timely to provide a consistent and simple nomenclature based on their known properties, both structural and functional. In 1995, Liscum and Briggs identified a genetic locus, designated NPH1 (non-phototropic hypocotyl 1), which encodes a plasma membrane–associated protein known to be essential for most phototropic responses in Arabidopsis. The phototropism mutant JK224, previously described by Khurana and Poff (1989), turned out to be mutated at the NPH1 locus. When plasma membrane preparations from dark-grown seedlings are irradiated before adding ATP, a 120-kD plasma membrane protein becomes heavily phosphorylated. This protein is present at most in trace amounts in the mutant JK224 (Reymond et al., 1992), providing genetic evidence for its role in phototropism. Cloning and sequencing of the NPH1 gene showed that the encoded protein contains all 11 classic motifs expected of a serine/threonine protein kinase (Hanks and Hunter, 1995), indicating that the protein itself was the kinase involved and that the light-activated reaction was an autophosphorylation event (Huala et al., 1997). When the protein was expressed in insect cells via Baculovirus transfection, it still retained light-activated phosphorylation, leading Christie et al. (1998) to conclude that it was itself the photoreceptor for the reaction and therefore a photoreceptor for phototropism. As a result, Christie et al. (1999) assigned the NPH1-encoded protein the trivial name “phototropin” after its functional role in phototropism. There are now a number of phototropin-like sequences in GenBank. (1) Jarillo et al. (1998) entered a sequence encoding a slightly smaller Arabidopsis protein with 58% identity and 67% similarity to phototropin. The gene was initially designated NPH2, but this was changed subsequently to NPL1 (NPH1-like 1) because the designation NPH2 was already used to describe another locus involved in phototropism (Liscum and Briggs, 1995). (2) Zacherl et al. (1998) entered sequences for two very similar NPH1 genes from Avena sativa (oat) designated NPH1-1 and NPH1-2. (3) These workers also have entered an NPH1 sequence from Zea mays (maize) (accession number AF033263). (4) Kanegae et al. (2000) reported two Oryza sativa (rice) NPH1-like genes that they designated OsNPH1a and OsNPH1b encoding proteins in rice (cv Nipponbare) that were 61 and 62% identical, respectively, to Arabidopsis phototropin at the protein level. The two genes show different tissue expression and differential regulation by light, suggesting that they might serve different functions. (5) Tyagi et al. (S.B. Tyagi, A.K. Tyagi, and J.P. Khurana, unpublished data) submitted an NPH1 homolog from a different strain of rice (Pusa Basmati 1) to GenBank (accession number CAB65325). (6) The Watson laboratory (R.V. Oakley, S.N. Chary, T. Mitra, and J.C. Watson, unpublished data) recently entered the complete sequence for the pea phototropin homolog PsPK4 (accession number U83281). (7) The Wada laboratory (Nozue et al., 2000) reported a gene with NPH1 homology from the fern Adiantum capillus-veneris. (8) Finally, Nozue et al. (1998) reported a novel chimeric protein from Adiantum. This protein has high homology with phytochrome (including a chromophore binding site and classic phytochrome photoreversibility) at its N-terminal end but with an almost complete phototropin homolog replacing the expected phytochrome sequence at its C-terminal end. These various genes and their GenBank accession numbers and pertinent references are listed in Table 1. (Note that the Arabidopsis NPL1, NPH2, and PK7 entries all report the same sequence.) Also included in Table 1is a phototropin-like gene from Chlamydomonas reinhardtii, its sequence kindly provided by Dr. Akira Nagatani, and a second phototropin homolog, NPL1, from Adiantum, its sequence kindly provided by Dr. Takatoshi Kagawa. Table 1also includes three fairly long partial sequences for apparent phototropin homologs that have been identified in Spinacia oleracea (spinach) (accession number Z30332), Mesembryanthemum crystallinum (ice plant) (Bauer et al., 1994), and Pisum sativum (pea) (Lin and Watson, 1992) that have been submitted to GenBank. Although GenBank contains other partial sequences that may represent phototropins, these