Light signalling

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Yoshikatsu Sato, Tadayoshi Hirai, Nagisa Sugimoto, and Tomoaki Nishiyama

(yoshi@nibb.ac.jp, tomoakin@kenroku.kanazawa-u.ac.jp)

Plants are sessile organisms and have established unique signalling pathway in response to light for their development during their life cycle (Chen, Chory, and Fankhauser 2004). Based on the phylogenetic trees, land plant orthologues were identified in all lineages for 43 of the 53 land plant orthologous group examined, which include 90 A. thaliana light signalling genes. It provides insights into the conservation of basic molecular mechanisms of the light signalling in land plants. Representative examples are COP10, DET1, DDB1A protein complex (CDD complex) and COP/DET/FUS genes which encode COP9 signalosome (CSN) subunits. The constant number of these genes during evolution may be due to exhibit multiple pairwise interactions between CSN subunits and form large complex. These two complexes function collaboratively with a COP1 E3 ubiquitin ligase in facilitating protein degradation. The system of the protein degradation mediated by COP/DET/FUS proteins was conserved in human. The blue light receptor, cryptochrome, directly interact with COP1 and inhibit degradation activity of COP1 against downstream transcription factors such as HY5, HYH, HFR1 and LAF1 in A. thaliana. A similar mechanism is proposed in the case of phytochrome A signalling. It is possible that plants innovate a way to de-etiolation by which photoreceptors have evolved to interact with COP1, because photoreceptor binding to COP1 seems to be plant specific. On the other hand, photoreceptors (phytochromes, cryptochromes, and phototropins) duplicated in each lineage in parallel as mentioned earlier studies (Lariguet and Dunand 2005, Mathews 2006). Early diverging of photoreceptors may be contributed to the functional divergence of each lineage in response to light environment. Actually, among PHYA specific signalling factors in A. thaliana, FAR1 and FHY3 genes, which encode transposase-related proteins and 12 additional FAR1-related genes designated as FRS1 to FRS12 were conserved only in angiosperm. These genes may be arisen by molecular co-evolution with PHYA signalling, because PHYA gene newly evolved in angiosperm. That may be also certainly the case with MYB trancription activator. The genes for both light perception and signal transduction were expanded in each lineage, suggesting that a range of modifications were made to the basic light signalling network in each lineage.


Contents

Photoreceptors

Phytocrome, cryptochrome, and phototropin

Phytochromes have small, multigene families with ancient evolutionary origins as mentioned earlier studies. With a notable exceptions, there is only one phytochrome gene but cryptocromes and phototropins extensively diverged in S. moellendorffii.


A list of A. thaliana genes whose potential orthologs were not found in other lineage

Found only in dicots UV-B LIGHT INSENSITIVE 3 (ULI3) encodes a protein that has potential domains for heme- and diacylglycerol-binding and function in UV-B light-mediated responses. We can not find potential orthologs of this gene in any lineage except A. thaliana, suggesting that ULI3 newly evolved in dicots.

COP1-INTERACTIVE PROTEIN 1 (CIP1) encodes a potentially coiled-coil structure protein that associates with the coiled-coil region of COP1. We can not find potential orthologs of this gene in any lineage except A.thaliana.

COP1-INTERACTIVE PROTEIN 4 (CIP4) encodes a nuclear protein and functions as a positive regulator of photomorphogenesis. We can not find potential orthologs of this gene in any lineage except A.thaliana.

Found only in flowering plants

PHYTOCHROME KINASE SUBSTRATE 1 (PKS1) encodes a basic soluble protein that can associate with PHYA or PHYB and is proposed to be a negative regulator of phyB signalling. We can not find PKS1 potential orthologs in S. moellendorffii and P. patens, suggesting that PKS1 newly evolved in angiosperm lineages.

MINI ZINC FINGER 1 (MIF1) was suggested to be involved in integrating signals from multiple hormones, such as abscisic acid, auxin, brassinosteroid, cytokinin, and gibberellic acid. Potential orthologs of this gene was found in angiosperm, but not in other land plant lineages, suggesting that MIF1 newly evolved in angiosperm and may function in mediating regulation of the plant development by multiple hormones.

Found only vascular plants

ZINC FINGER PROTEIN 1 (ZFP1) encodes a C2H2 zinc-finger protein and show light regulated expression in the shoot apex including the apical meristem, developing leaves and the developing vascular system. This gene was conserved in A. thaliana, O. sativa, and S. moellendorffii, but not P. patens, suggesting that this gene newly evolved in vascular plant lineage and may function in vascular development.

COP1-INTERACTING PROTEIN 8 (CIP8) encodes a RING-H2 protein that associates with the RING finger domain of COP1. CIP8 facilitate degradation of HY5, positive regulater of photomorphogenesis. This gene was conserved in A. thaliana, O. sativa, and S. moellendorffii, but not P. patens, suggesting that this gene newly evolved in vascular plant lineage.

Not found in monocots

SHORT HYPOCOTYL UNDER BLUE 1 (SHB1) encodes a protein that has SYG1 protein conserved motifs and acts in cryptochrome signalling. and phyA-mediated far-red responses. SHB1 gene more extensively diverged in dicots than in other lineages. We found SHB1 potential orthologs in S. moellendorffii and P. patens, but not in O. sativa

Table of gene numbers

Gene functions Gene Gene used as a query The number of putative orthologs
Arabidopsis thaliana Oryza sativa Selaginalla moellendorffii (a) Physcomitrella patens
Light signalling PHYA to E PHYA 5 3 1 (1) 8
Light signalling CRY1, 2 CRY1 2 3 3 (6) 2
Light signalling CRY3 CRY3 1 1 1 (2) 1
Light signalling PHOT1 and 2 PHOT1 2 2 2 (4) 6
Light signalling HO1 to 4 HO3 4 2 1 (1) 5
Light signalling HY2 HY2 1 1 1 (2) 1
Light signalling PAT1 PAT1 6 6 1 (1) 2
Light signalling EID1 EID1 1 1 1 (2) 3
Light signalling LAF3 LAF3 1 1 2 (4) 1
Light signalling FAR1, FRS1 to 12, and FHY3 3) FAR1 14 56 0 0
Light signalling FHY1 FHY1 1 2 1 (2) 1
Light signalling PIF1/PIL5, PIF3 and 4, PIL1 to 4, and HFR/PIL6 PIL6 14 10 3 (6) 3
Light signalling NDPK1 NDPK2 1 2 1 (2) 2
Light signalling NDPK2 NDPK2 1 1 1 (2) 2
Light signalling PP5 PP5 1 1 1 (1) 2
Light signalling PP7 PP7 3 1 3 (5) 3
Light signalling ATFYPP3 ATFYPP3 2 1 1 (2) 2
Light signalling HRB1 HRB1 7 7 4 (7) 4
Light signalling SHL1 SHL1 3 4 2 (3) 6
Light signalling SUB1 SUB1 3 3 2 (3) 1
Light signalling NPH3 NPH3 2 1 3 (6) 15
Light signalling RPT2 RPT2 8 5 4 (8) 4
Light signalling JAC1 JAC1 7 5 4 (8) 4
Light signalling PKS1 PKS1 4 1 0 0
Light signalling CDF1 CDF1 7 6 3 (4) 4
Light signalling SHB1 SHB1 9 0 3(6) 2
Light signalling COP1 SPA1 1 1 1 (2) 9
Light signalling COP10/FUS9 COP10 1 1 1 (1) 2
Light signalling CIP8 CIP8 6 3 2 (4) 0
Light signalling SPA1 to 4 SPA1 4 2 1 (2) 2
Light signalling CIP1 CIP1 1 0 0 0
Light signalling CIP4 CIP4 2 0 0 0
Light signalling CIP7 CIP7 6 3 5 (9) 2
Light signalling HY5 and HYH HY5 2 3 2 (4) 2
Light signalling LAF1 LAF1 3 3 0 0
Light signalling DET1/FUS2 DET1 1 1 1 (2) 3
Light signalling DDB1A DDB1A 2 1 1 (1) 2
Light signalling COP11/FUS6 COP11 1 1 1 (2) 2
Light signalling COP12/FUS12 FUS12 1 1 1 (2) 3
Light signalling COP13/FUS11 FUS11 1 1 1 (2) 1
Light signalling COP8/FUS4/FUS8 COP8 1 1 1 (2) 1
Light signalling AJH1 and 2 AJH2 2 1 1 (2) 2
Light signalling CSN6A and B CSN6A 2 4 1 (2) 2
Light signalling COP15/FUS5 FUS5 1 1 1 (2) 2
Light signalling COP9/FUS7 COP9 1 2 1 (2) 1
Light signalling AMP1 AMP1 2 4 4 (7) 2
Light signalling PFT1 PFT1 1 1 2 (3) 2
Light signalling TED3 TED3 1 1 1 (2) 1
Light signalling OBP3 OBP3 13 4 0 0
Light signalling HLS1 HLS1 4 4 1 (2) 2
Light signalling CR88 CR88 2 2 1 (1) 2
Light signalling MIF1 MIF1 3 3 0 0
Light signalling ZFP1 ZFP1 27 27 6 (11) 10

footnote: The number of putative orthologs here refers to number of genes that is included in a clade that corresponds to all genes derived from a single gene in the last common ancestor of P. patens, S. moellendrffii, A. thaliana, and O. sativa based on phylogenetic analyses. The alignments and trees are available through http://moss.nibb.ac.jp/treedb/ (a) number of putative loci at first and number of putative alleles detected in parentheses. That is, 1 (2), indicates we found two sequences that likely represent two alleles of one locus. See http://wiki.genomics.purdue.edu/index.php/Evolution_of_developmental_genes#Methods for brief methods.

Table of gene models in the assembly

protein id gene name annotated by
PHYTOCHROMES
161430 PHYTOCHROME-1
161807 PHYTOCHROME-2
Cryptochrome related genes
75166 CRY1-1
91442 CRY1-2
142524 CRY2-1
967 CRY2-2
92414 CRY3-1
114313 CRY3-2
106065 CryD-1
268379 CryD-2
Phototropins
230655 PHOT1-1
10296 PHOT1-2
172224 PHOT2-1
186203 PHOT2-2
97989 HO-1
83654 HY2-1 Yoshikatsu Sato
151708 HY2-2 Yoshikatsu Sato
449932 PAT1-1
95139 PAT1-2
127090 EID1-1 Tadayoshi Hirai
133264 EID1-2 Tadayoshi Hirai
164034 LAF3A-1
451266 LAF3A-2
166701 FHY1-1 Tadayoshi Hirai
186552 FHY1-2 Tadayoshi Hirai
171292 NDPK1-1
109077 NDPK1-2
174713 NDPK2-1 Yoshikatsu Sato
443584 NDPK2-2 Yoshikatsu Sato
270355 NDPK3-1
228272 NDPK3-2
182535 PP5-1
185525 PP5-2 Tadayoshi Hirai
426688 PP7A-1
185987 PP7A-2
12808 PP7B-1
429646 PP7B-2
451287 PP7C-1
232099 FYPP3-1
270060 FYPP3-2
100159 PPX-1
118556 PPX-2
405842 HRB1A-1
451294 HRB1A-2
447111 HRB1B-1
451288 HRB1B-2
451290 HRB1C1-1
16505 HRB1C2-1
451293 HRB1C1-2
412601 SHL1A-1
431611 SHL1A-2
420725 SHL1B-1
445241 SHL1B-2
81611 SUB1A-1
128681 SUB1A-2
84756 SUB1B-1
104607 SUB1B-2
166345 NPH3A-1
183709 NPH3A-2
93693 NPH3B-1
108722 NPH3B-2
90150 NPH3C-1
51551 NPH3C-2
171333 COP1-1
176960 COP1-2
141846 COP1L1-1
101639 COP1L1-2
451298 COP1L2-1
451299 COP1L2-2
98534 SPA1-1
181056 SPA1-2
231529 RPT2A-1
443843 RPT2A-2
74933 RPT2B-1
118052 RPT2B-2
141980 RPT2C-1
447227 RPT2C-2
228979 RPT2D-1
272040 RPT2D-2
451301 JAC1L1-1
451303 JAC1L1-2
447002 JAC1L2-1
448911 JAC1L2-2
445035 JAC1L3-1
432122 JAC1L3-2
451314 JAC1L4-1
451308 JAC1L4-2
440428 CDF1A-1
443038 CDF1A-2
437759 CDF1B-1
444655 CDF1B-2
448037 CDF1C-1
61168 SHB1A-1
134638 SHB1A-2
405792 SHB1B-1
134575 SHB1B-2
430278 SHB1C-2
449731 COP10-1 Michael Gribskov
449734 COP10-2 Michael Gribskov
451319 CIP8A-1
429694 CIP8A-2
451322 CIP8B-1
451325 CIP8B-2
440988 HY5A-1
451326 HY5A-2
173274 HY5B-1
451330 HY5B-2
167525 DET1-1 Yoshikatsu Sato
104399 DET1-2 Yoshikatsu Sato
145521 DDB1-1 Yoshikatsu Sato
151061 DDB1-2 Yoshikatsu Sato
235966 FUS6-1
135331 FUS6-2
146093 PSD6-1
267709 PSD6-2
170816 FUS12-1 Nagisa Sugimoto
147370 FUS12-2 Nagisa Sugimoto
439255 COP13-1 Nagisa Sugimoto
162886 COP13-2 Nagisa Sugimoto
165253 COP8-1 Nagisa Sugimoto
82579 COP8-2 Nagisa Sugimoto
73440 JAB1-1
168868 JAB1-2
74712 CSN6-1 Yoshikatsu Sato
230963 CSN6-2 Yoshikatsu Sato
179250 FUS5-1 Yoshikatsu Sato
123333 FUS5-2 Yoshikatsu Sato
143083 COP9-1
182492 COP9-2
421595 AMP1A-1
134963 AMP1A-2
81471 AMP1B-1
88219 AMP1B-2
73556 AMP1C-1
119241 AMP1C-2
86742 AMP1D1-2
87649 AMP1D2-2
61588 AMP1D3-1
61589 AMP1D1-1
402884 AMP1D2-1
440592 PFT1A-1
442372 PFT1A-2
405603 PFT1B-1
408814 PFT1B-2
413661 TED3-1
416594 TED3-2
231183 HLS1-1
104443 HLS1-2
88538 CR88-1
448838 CR88-2
451343 SHD-1
444847 SHD-2
405785 ZFP1a-1
450816 ZFP1b-1
450814 ZFP1b-2
409409 ZFP1c-1
416162 ZFP1c-2
450832 ZFP1d-1
450839 ZFP1d-2
research Groups