Discussion Although phyA is one of the best characterized photoreceptors in higher plants, the protein components involved in the signal transduction pathway are just beginning to emerge ( Deng and Quail 1999; Smith 2000; Neff et al. 2000; Fankhauser 2001; Nagy et al. 2001). Isolation and characterization of mutants, especially from Arabidopsis, has proven to be one of the most powerful tools in dissecting the phyA signaling pathway. laf1 is a novel mutant specific for the phytochrome A signal transduction pathway Here, we report the genetic identification of a LAF1, which is involved in phyA signal transduction. The most obvious phenotype of laf1 is the reduced inhibition of hypocotyl elongation when germinated under FR light. LAF1 is a specific phyA signaling intermediate as the hypocotyl length is not affected under any other light condition. This is underscored by the molecular analysis, which showed that expression of CHS, CAB, PET E, and XTR7 is only affected in a phyA-dependent way. The genetic analysis performed here indicates that LAF1 is not allelic to photomorphogenic mutants reported previously. The genetic evidence also indicates that the laf1 mutation is recessive, and that the insertion of a Ds element into the third exon of the gene caused a complete loss-of-function mutation, as no LAF1 transcript can be detected in the mutant. Nevertheless, laf1 is not completely blocked in phyA signaling, because the hypocotyl elongation is still responsive to FR light and even under low FR light the hypocotyl is not as long as that of a phyA mutant. Under higher FR light fluencies laf1 seedlings are also sensitive to the FR-killing effect, which they are not under low fluencies (<2 μmole/m 2 sec). This fluence dependency is confirmed by hypocotyl length analysis (Fig. 2C) and the CAB gene expression pattern (Fig. 3). Furthermore, the laf1 mutant is affected only in a subset of phyA-mediated responses, as under FR light hook opening is not impaired, cotyledons are completely unfolded and expanded (Fig. 1B), and the seedlings show no loss of FR-dependent gravitropism. As the loss of LAF1 in this null mutant leads to a reduction in phyA signaling, LAF1 must be either an integral component of the transduction pathway or a positive regulator of it. The results suggest that LAF1 could be an element of a pathway that contributes only to some aspects of de-etiolation and needs to act in concert with other pathways for full effect. On the other hand, the partial block of signaling can be explained by the fact that other proteins might have overlapping functions with LAF1; therefore, the loss of LAF1 has only a mild effect on physiological responses. LAF1 appears to be more important at lower FR fluencies compared with high fluencies. LAF1 could be rate limiting at low FR light intensities, but at higher light intensities other factors might be able to substitute. This also might explain why the phenotype is not as strong as in the phyA mutant. LAF1, a R2R3–MYB protein, acts as a transcriptional activator The LAF1 gene encodes a protein with sequence homology with the large R2R3–MYB protein family ( Romero et al. 1998), corresponding to AtMYB18, previously named by Kranz et al. (1998). The constitutive nuclear localization of transiently expressed LAF1 in onion epidermal cells and the presence of the putative DNA binding domain suggest that LAF1 might act as a transcription factor. We tested whether LAF1 can transactivate a reporter gene when fused to the DNA binding domain of GAL4. The results showed that the domain necessary for transactivation is located in the C terminus of the protein (amino acids 164–283) and especially between amino acid 217 and the C terminus. In other MYB transcription factors, this region also has been shown to be important for transactivation, although no sequence homology is apparent ( Lee and Schiefelbein 1999). These results suggest that LAF1 might be involved in the fine tuning of a certain subset of genes as a transcription factor. Although we understand well how MYB factors bind to target DNA ( Rosisnsky and Atchley 1998), little is known about their functions. In vertebrates, for example, many MYB proteins have been found to play an essential regulatory role in cell proliferation and differentiation ( Thompson and Ramsay 1995). The functions of MYB genes in plants appear to be far more diverse. Several members have been implicated in the regulation of secondary metabolism, cellular morphogenesis or the control of cell differentiation and cell cycle, signal transduction in plant growth, and responses to hormones, stress, and defense ( Jin and Martin 1999). To our knowledge, this report describes the first R2R3–MYB transcription factor shown to be involved in light signal transduction. So far, few transcription factors have been shown to function in light signaling in Arabidopsis. PIF3 and RSF1/HFR1/REP1 each contain a bHLH motif ( Ni et al. 1998; Fairchild et al. 2000; Soh et al. 2000; Spiegelman et al. 2000), CCA1 and LHY1 each contain a single MYB domain ( Wang et al. 1997; Schaffer et al. 1998), and HY5 is a bZIP ( Oyama et al. 1997). PIF3 was identified as a phytochrome-interacting factor in a yeast two-hybrid screen. Bound to a DNA target site, PIF3 can interact directly with phytochrome in the Pfr form in vitro, suggesting that one mode of phytochrome signal transduction is the direct transcriptional regulation of target genes ( Martinez-Garcia et al. 2000). Although PIF3 originally was identified as a protein interacting with both phyA and phyB, more recent biochemical and physiological data suggest that PIF3 plays a more prominent role in phyB signaling than in phyA signaling ( Halliday et al. 1999; Zhu et al. 2000). In contrast, based on their respective loss-of-function phenotypes, RSF1/HFR1/REP1 and LAF1 are implicated in phyA signaling, but not phyB signaling. The effect of the laf1 mutation on CAB, PET E, CHS, and XTR7 gene expression does not allow the distinction whether LAF1 has a direct or indirect impact on the transcription of these genes. The difference in the gene expression pattern of laf1 as compared with WT is more pronounced after 18 h than after 2 h incubation in FR. This suggests that LAF1 might control the sustained transcription of these genes under FR light. A similar observation has been made in the rep1 mutant, where at the 3-h time point the induction of CAB gene expression is similar to WT, but after 6 h the induction is strongly reduced ( Soh et al. 2000). LAF1 localizes to nuclear speckles Recent studies have shown that besides transcriptional regulation, post-translational modifications such as phosphorylation or protein degradation also play critical roles in the regulation of plant transcription factors ( Callis and Vierstra 2000; Hardtke and Deng 2000). One indication that LAF1 accumulation or activity might be regulated is that transgenic plants overexpressing a 35S–LAF1 transgene do not show any obvious phenotype nor any hypersensitivity to FR light, although the LAF1 transcript levels are elevated (Fig. 2C). One interesting observation is that the LAF1 protein not only localizes to the nucleus, but is directed to distinct nuclear speckles in a time-dependent manner. Nuclear speckles are formed for different reasons. One class of speckles is localized within the interchromatin space and enriched in splicing factors ( Lewis and Tollervey 2000). Nuclear speckles also have been implicated in protein modifications caused by SUMO, a small ubiquitin-like modifier, which is conjugated to target proteins by an isopeptide bond ( Melchior 2000; Müller et al. 2001). In contrast with ubiquitination, however, the covalent attachment of SUMO does not lead to protein degradation. Only a few SUMO target proteins have been identified, and so far, to our knowledge, none in plants. The exact function of SUMO modification, or sumoylation, is not known. In some cases (e.g., IκBα and p53), conjugation of SUMO could lead to protein stabilization and protection from degradation, whereas in other cases (PML, SP100, RanGAP1, and HIPK2), SUMO conjugation could lead to a different subcellular localization of the modified protein, especially to nuclear speckles (summarized in Melchior 2000; Müller et al. 2001). Surprisingly, many SUMO targets, such as RanGAP1, PML, and HIPK2, contain PEST sequences, which are stretches of at least 12 amino acids rich in P, E, D, S, or T but lacking positively charged amino acids ( Rechsteiner and Rogers 1996). In LAF1, two putative PEST sequences can be identified (Fig. 5). The covalent modification of a target protein by SUMO has been shown to occur at a lysine residue within a minimal consensus sequence, Ψ KX(E,D) ( Melchior 2000; Rodriguez et al. 2001). LAF1 contains the sequence K KQE (257–260), which is a good match with the consensus sequence, although lacking the hydrophobic amino acid. On changing K258 to R258, thereby disrupting the putative SUMO conjugation site, we observed diffuse nuclear staining and rare speckle formation. These results suggest that recruitment of LAF1 to nuclear speckles requires K258, and this lysine might act as a modification site for SUMO. The domain that is important for nuclear speckle localization is distinct from the nuclear localization signals, which are in the N-terminal portion. However, the C-terminal sequence, containing the domain with the putative sumoylation signal is not sufficient for targeting to nuclear speckles. An SV40 NLS fused to LAF1/171–283 directed the protein to the nucleus but not to speckles. It appears that a functional DNA-binding domain is needed for localization of LAF1 to nuclear speckles. So far, the only plant proteins that have been identified to localize to speckles are COP1, all phytochromes, CRY2, a blue-light photoreceptor, and RPN6, a component of the proteasome ( von Arnim et al. 1998; Mas et al. 2000; Nagy et al. 2001; Peng et al. 2001). COP1 is a RING-finger protein with WD-40 repeats acting as a negative regulator of photomorphogenic development. The COP1 protein has been compared with PML because of their conserved domain structure and similar localization to speckles ( Reyes 2001). Analysis of COP1 deletion mutants identified a 50-amino-acid long domain (SNLS) that is necessary for the localization in speckles ( Stacey and von Arnim 1999). Although this domain shows no obvious homology with LAF1, it contains a putative sumoylation signal, R KME. In summary, we present molecular and genetic evidence that LAF1, a nuclear protein containing two MYB motifs, is necessary for a branch of phyA signaling that regulates various photoresponses, including inhibition of hypocotyl elongation as well as CAB, PET E, XTR7, and CHS gene expression. The localization of LAF1 suggests an evolving theme that transcription factors are regulated on the level of protein stability and/or partitioning. Further analysis of the genes that are regulated by LAF1, and the factors that interact with LAF1 should provide important clues for identifying molecular intermediates, which lead from phytochrome photoconversion to alterations in gene expression. |
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