Light perception. phytochromes, cryptochromes, phototropins.
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1 Light perception phytochromes, cryptochromes, phototropins. all photoreceptors consist of proteins bound to light absorbing pigments i.e. chromophores. the spectral sensitivity of each photoreceptor depends on its chromophore s ability to absorb different wavelengths i.e. on the chromophore s absorption spectrum. in response to light absorption, downstream signaling is mediated by the photoreceptor protein.
2 Development of Arabidopsis seedling is strongly dependent on light
3 Phytochromes 120 kda protein family TKDs transmitter kinase domains HKLD prokaryotic histidine kinase like domain (Quail 2002) Absorption spectra of phytochromes Li et al., (2011) Arabidopsis Book
4 Plants Respond to Light Photomorphogenesis, Phototropism, Photoperiodism Phytochrome responses (red/far red) flowering and dormancy; branch patterns; root growth Blue light responses stomatal opening; phototropism; chloroplast orientation
5 A light perception system is critical for the meaningful regulation of plant metabolism Plants use photoreceptors to detect environmental light changes These act as initiators of signal transduction cascades that ultimately direct plant s response to light level Most light responses are controlled by chromoproteins They contain a chromophore absorbs light They are an apoprotein undergoes conformational change (initiates signal transduction cascade)
6 What Is Phytochrome? Phytochrome is a pigment found in some plant cells that has been proven to control plant development. This pigment has two forms or phases in can exist in. P-red light sensitive (Pr) and P far red light sensitive (Pfr) forms. The actual plant response is very specific to each specie, and some plants do not respond at all.
7 Photoconversion and Dark reversion 660 nm Synthesis Pr Red Light (Fast) Far Red Light Dark Reversion Pfr 740 nm Destruction Vegetative (Non-Flowering) (Slow) Reproductive (Flowering)
8 The structure of Phytochrome A dimer of a 1200 amino acid protein with several domains and 2 molecules of a chromophore. Chromophore 660 nm 730 nm Pr Pfr Binds to membrane
9 Low fluence responses are the most studied changes induced by phytochrome These regulate important plant growth and development responses including De-etiolation the greening of etiolated seedlings Important as seedlings emerge from the soil and begin to become autotrophic Seed germination breaking of seed coat, start of active metabolism in new plant Light can promote or inhibit germination, depending on the species
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12 Regulation of photomorphogenesis genes Li et al., (2011) Arabidopsis Book
13 (A) The biosynthesis pathway of Arabidopsis phytochrome chromophore For plants, the sensing of light in the environment is as important as vision is for animals. Fluctuations in light can be crucial to competition and survival. One way plants sense light is through the phytochromes, a small family of diverse photochromic protein photoreceptors whose origins have been traced to the photosynthetic prokaryotes. During their evolution, the phytochromes have acquired sophisticated mechanisms to monitor light. Recent advances in understanding the molecular mechanisms of phytochromes and their significance to evolutionary biology make possible an interim synthesis of this rapidly advancing branch of photobiology. Li et al., (2011) Arabidopsis Book
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15 The domain structure of Arabidopsis phya and phyb molecules GAF, cgmp-stimulated phosphodiesterase PHY, phytochrome; PRD, PAS-related domain; HKRD, histidine kinase related domain. The chromophore is attached to a conserved cysteine residue in the GAF domain. The numbers indicate the positions of each domain. Bae and Choi (2008)
16 Smith (2000) Nature
17 Phytochrome function Li et al., (2011) Arabidopsis Book
18 phytochrome action Phytochromes undergo photoconversion from the biologically inactive form (Pr) to the active form (Pfr). Pr and Pfr are shown as dimers in the cell. The diagram shows the three major theories for the subsequent actions of the phytochromes, although Pfr may regulate growth and development by other processes. Pink area: both Pr and Pfr interact with PKS1, the phytochrome kinase substrate, in the cytosol. This may be the first step in a kinase cascade (orange area) culminating in action within the cytoplasm. Alternatively, interaction with PKS1 may result in sequestration of phytochrome in the cytosol, preventing translocation to the nucleus. Yellow area: Pfr interacts with NDPK1, a nucleoside diphosphate kinase, which is located both in the cytoplasm and the nucleus. Again, this interaction may initiate a kinase cascade (orange) leading to ultimate action within the cytoplasm and/or nucleus. Green area: Pfr translocates to the nucleus and Pr is translocated back to the cytoplasm. The weights of the arrow emphasize the differential rates of import and export. Within the nucleus, Pfr binds with PIF3 (phytochrome interacting factor 3) which is located exclusively within the nucleus. PIF3 is a basic helix loop helix transcription factor that binds to the promoters of selected light-regulated genes in combination with Pfr and initiates or enhances transcription. Smith (2000) Nature
19 Seedling De-etiolation Dark-grown seedlings (skotomorphogenesis): etiolation, long hypocotyls, closed cotyledons and apical hooks, and development of the proplastids into etioplasts. Light-grown seedlings (photomorphogenesis): deetiolation, short hypocotyls, open and expanded cotyledons, and development of the proplastids into green mature chloroplasts (McNellis and Deng, 1995). Phytochromes perform a variety of overlapping functions in regulating seedling de-etiolation. 1. Mutants deficient in phya display a wild-type photomorphogenic phenotype in W and R light. 2. when grown in continuous FR light, phya mutants display a skotomorphogenic phenotype, confirming that phya is the primary photoreceptor responsible for perceiving and mediating various responses to FR light (Dehesh et al, 1993) 3. phyb is the predominant phytochrome regulating de-etiolation in W and R light Phenotypes of 4-d-old wild-type (WT), phya, phyb and phya phyb mutant plants grown in darkness (D) or under continuous white (W), far-red (FR), red (R) and blue (B) light conditions. Li et al., (2011) Arabidopsis Book
20 Phenotypes of 3-week-old wild-type (WT), phya, phyb, phya phyb, phyb phyd phye, phya phyb phyd phye plants grown under white light conditions (16-h light/8-h dark). Li et al., (2011) Arabidopsis Book
21 LIGHT-REGULATED SUBCELLULAR LOCALIZATION OF PHYTOCHROMES light-regulated translocation of the photoreceptors from the cytoplasm into the nucleus is a key event in the phytochrome signaling cascade. Regulation of phya Nuclear Localization The nuclear accumulation pattern of phya is quite distinct from that of phyb. Firstly, all light illuminations (FR, R and B) are effective in inducing phya nuclear translocation. A single, brief pulse of FR, R or B light induces phya nuclear import as well (Hisada et al., 2000) phya nuclear translocation is very rapid (within minutes), whereas phyb nuclear import is relatively slow that takes hours. in contrast to phyb-phye, phya is exclusively localized in the cytosol in etiolated seedlings (Kircher et al., 2002). phyb nuclear accumulation is efficiently initiated by continuous R light, and to a lesser extent by continuous B light, but completely ineffective by FR light. Single pulses of R, FR and B light cannot induce phyb nuclear accumulation (Gil et al., 2000). phyb nuclear transport by R light is reversible by FR light
22 Control of FHY1/FHL expression and phya nuclear accumulation FHY1 and FHL are required for phya nuclear accumulation (Hiltbrunner et al., 2005, 2006; Genoud et al., 2008). FHY3 and FAR1 are two transposase-derived transcription factors that directly activate FHY1/FHL transcription, and thus indirectly regulate phya nuclear accumulation and subsequent responses (Lin et al., 2007). phya is localized exclusively in the cytosol in darkness in its inactive Pr form. Upon light exposure, the Pfr form of phya is imported into the nucleus by FHY1/FHL, and thus triggers phya signaling leading to multiple light responses, including the reduction of COP1 in the nucleus and accumulation of HY5 (Osterlund and Deng, 1998; Osterlund et al., 2000), and feedback regulation of FHY3 and FAR1 transcript levels (Lin et al., 2007). HY5 plays dual roles in phya signaling: promoting photomorphogenesis, and down-regulating FHY1/FHL transcript levels by modulating the activities of the transcriptional activators FHY3 and FAR1 (Li et al., 2010). Li et al., (2011) Arabidopsis Book
23 Structural comparison of Arabidopsis phytochromes and the bacterial phytochrome Cph1 HKD, histidine kinase domain. The percent amino acid identities between the HKD domain of Cph1 and both PRD and HKRD domains of Arabidopsis phytochromes are indicated. (adapted from Yeh and Lagarias, 1998).
24 Dark-grown cop1 mutant seedlings phenotypically mimic light-grown wild-type seedlings
25 A simplified model of the phytochrome signaling pathway phya is the primary photoreceptor responsible for perceiving and mediating various responses to FR light phyb is the predominant phytochrome regulating responses to R light. Under light conditions, these photoreceptors act to suppress two main branches of light signaling: COP1-TFs and PIFs. COP1, whose activity is repressed by phytochromes in light conditions, is an E3 ubiquitin ligase targeting several photomorphogenesispromoting transcription factors (such as HY5, HYH, LAF1 and HFR1) for degradation. PIFs are a subset of bhlh transcription factors required for skotomorphogenesis. Photo-activated phytochromes directly interact with PIFs, resulting in PIFs' phosphorylation and degradation while COP1 positively regulates PIFs' protein levels. Phytochromes are targeted for degradation by COP1, and PIFs contribute to the degradation of phyb by promoting COP1/phyB interaction. adapted from Lau and Deng (2010).
26 Seedling De-etiolation Dark-grown seedlings (skotomorphogenesis): etiolation, long hypocotyls, closed cotyledons and apical hooks, and development of the proplastids into etioplasts. Light-grown seedlings (photomorphogenesis): deetiolation, short hypocotyls, open and expanded cotyledons, and development of the proplastids into green mature chloroplasts (McNellis and Deng, 1995). Phytochromes perform a variety of overlapping functions in regulating seedling de-etiolation. 1. Mutants deficient in phya display a wild-type photomorphogenic phenotype in W and R light. 2. when grown in continuous FR light, phya mutants display a skotomorphogenic phenotype, confirming that phya is the primary photoreceptor responsible for perceiving and mediating various responses to FR light (Dehesh et al, 1993) 3. phyb is the predominant phytochrome regulating de-etiolation in W and R light Phenotypes of 4-d-old wild-type (WT), phya, phyb and phya phyb mutant plants grown in darkness (D) or under continuous white (W), far-red (FR), red (R) and blue (B) light conditions. Li et al., (2011) Arabidopsis Book
27 Schematic Model for the Role of Tyrosine Phosphorylation at Amino Acid 104 in phyb Signaling Nito et al., (2013) phyb is synthesized in its Pr form and remains in the cytoplasm in dark-grown seedlings. After red light exposure, Pr is rapidly converted to Pfr and translocates into the nucleus to promote degradation of PIFs for photomorphogenesis. The site of this interaction is likely to be in nuclear bodies. Depending on light conditions, Excess Pfr form of phyb is phosphorylated at Y104 to inactivate phyb and phyb signaling is relieved regardless of its photochemical states. phyb with the phosphotyrosine cannot interact with PIFs. The phosphorylation on Y104 seems not to affect nuclear import of phyb, however it is still unclear at where Y104 is phosphorylated in the cell. To reactivate the phosphorylated phyb, protein tyrosine phosphateses (PTPs) may need to dephosphorylate Y104 on phyb.
28 FLC-promoted germination involves the ABA catabolic pathway (via CYP707A2) and GA biosynthetic pathway (via GA20ox1) in seeds. (A) Proportion of viable seed germination (±1 SE). C, control; U, uniconazol; F, flouridone; U+F, uniconazol + flouridone. Asterisks indicate significant differences between WT and their respective NIL or 35S::FLC overexpressor. (B) The expression (±1 SE) of CYP707A2 in NIL-FLCCvi and Ler seeds at different stages. (C) Expression of GA20ox1 (±1 SE) at different stages. (D) Simplified pathway model of the hypothesized connections between flowering and germination pathways, and the possible signal transduction during flowering (Left) and germination (Right). AP1 repression by high FLC expression during seed development directly or indirectly influences CYP707A2 and GA20ox1 through unknown pathways in germinating seeds. Chiang et al., (2009) PNAS 106:
29 LIGHT-REGULATED SUBCELLULAR LOCALIZATION OF PHYTOCHROMES light-regulated translocation of the photoreceptors from the cytoplasm into the nucleus is a key event in the phytochrome signaling cascade. Regulation of phya Nuclear Localization The nuclear accumulation pattern of phya is quite distinct from that of phyb. Firstly, all light illuminations (FR, R and B) are effective in inducing phya nuclear translocation. A single, brief pulse of FR, R or B light induces phya nuclear import as well (Hisada et al., 2000) phya nuclear translocation is very rapid (within minutes), whereas phyb nuclear import is relatively slow that takes hours. in contrast to phyb-phye, phya is exclusively localized in the cytosol in etiolated seedlings (Kircher et al., 2002). phyb nuclear accumulation is efficiently initiated by continuous R light, and to a lesser extent by continuous B light, but completely ineffective by FR light. Single pulses of R, FR and B light cannot induce phyb nuclear accumulation (Gil et al., 2000). phyb nuclear transport by R light is reversible by FR light
30 Control of FHY1/FHL expression and phya nuclear accumulation FHY1 and FHL are required for phya nuclear accumulation (Hiltbrunner et al., 2005, 2006; Genoud et al., 2008). FHY3 and FAR1 are two transposase-derived transcription factors that directly activate FHY1/FHL transcription, and thus indirectly regulate phya nuclear accumulation and subsequent responses (Lin et al., 2007). phya is localized exclusively in the cytosol in darkness in its inactive Pr form. Upon light exposure, the Pfr form of phya is imported into the nucleus by FHY1/FHL, and thus triggers phya signaling leading to multiple light responses, including the reduction of COP1 in the nucleus and accumulation of HY5 (Osterlund and Deng, 1998; Osterlund et al., 2000), and feedback regulation of FHY3 and FAR1 transcript levels (Lin et al., 2007). HY5 plays dual roles in phya signaling: promoting photomorphogenesis, and down-regulating FHY1/FHL transcript levels by modulating the activities of the transcriptional activators FHY3 and FAR1 (Li et al., 2010). Li et al., (2011) Arabidopsis Book
31 A simplified model of the phytochrome signaling pathway phya is the primary photoreceptor responsible for perceiving and mediating various responses to FR light phyb is the predominant phytochrome regulating responses to R light. Under light conditions, these photoreceptors act to suppress two main branches of light signaling: COP1-TFs and PIFs. COP1, whose activity is repressed by phytochromes in light conditions, is an E3 ubiquitin ligase targeting several photomorphogenesispromoting transcription factors (such as HY5, HYH, LAF1 and HFR1) for degradation. PIFs are a subset of bhlh transcription factors required for skotomorphogenesis. Photo-activated phytochromes directly interact with PIFs, resulting in PIFs' phosphorylation and degradation while COP1 positively regulates PIFs' protein levels. Phytochromes are targeted for degradation by COP1, and PIFs contribute to the degradation of phyb by promoting COP1/phyB interaction. adapted from Lau and Deng (2010).
32 Predicted Phosphorylation Sites on phyb by Mass Spectrometry Analysis (A) Top panel: the full-length A. thaliana phyb structure. The N-terminal half is separated into four regions designated the N, PLD, GAF, and PHY domains. Two PAS domains and histidine kinase-related domain (HKRD) are located in the C-terminal half. Star: chromophore-binding site. The graphs depict the frequency of predicted phosphorylation by mass spectrometry analysis before (0 hr) and after (6 hr) white-light treatment. The gray box indicates putative light-dependent phosphorylation cluster in the N terminus. (B) Bottom graph: enlarged aa region of 6-hrexposed phyb. Six groups of putative sites (S84,S86, T89 T91, S94,S95, Y104, S106, and Y113) are indicated. (C) Comparison of the PCSM motif in phytochromes from various species. Alignment of amino acid sequences was calculated with ClustalW software. Phosphorylation sites S84,S86, T89-T91, Y104, and S106 are indicated. Gray box indicates bacterial phytochromes. Nito et al., (2013)
33 phyb Y104F Cannot Complement phyb-9 Null Mutant (A) Seedlings grown under the long-day condition with white light for 7 days. Col-0; phyb-9; WT, expressing phyb WT ; Y104F, nonphospho mutant phyb Y104F ; Y104E, phosphomimic mutant phyb Y104E. (B) Hypocotyl measurement under different red-light intensities. Two representative transgenic lines were analyzed from each line. Col-0; phyb-9; WT, expressing phyb WT ; Y104F, nonphospho mutant phyb Y104F ; Y104E, phosphomimic mutant phyb Y104E. Error bar is SE (n = 30). (C) Thirty-day-old plants of phospho mutants of Y104, grown under long-day conditions. Col-0; phyb-9; P 35S ::PHYB-CFP, phyb-cfp overexpressor; native promotor lines (P PHYB ::PHYB-mCitrine) of WT, expressing phyb WT ; Y104F, nonphospho mutant phyb Y104F ; Y104E, phosphomimic mutant phyb Y104E. Nito et al., (2013)
34 Schematic Model for the Role of Tyrosine Phosphorylation at Amino Acid 104 in phyb Signaling Nito et al., (2013) phyb is synthesized in its Pr form and remains in the cytoplasm in dark-grown seedlings. After red light exposure, Pr is rapidly converted to Pfr and translocates into the nucleus to promote degradation of PIFs for photomorphogenesis. The site of this interaction is likely to be in nuclear bodies. Depending on light conditions, Excess Pfr form of phyb is phosphorylated at Y104 to inactivate phyb and phyb signaling is relieved regardless of its photochemical states. phyb with the phosphotyrosine cannot interact with PIFs. The phosphorylation on Y104 seems not to affect nuclear import of phyb, however it is still unclear at where Y104 is phosphorylated in the cell. To reactivate the phosphorylated phyb, protein tyrosine phosphateses (PTPs) may need to dephosphorylate Y104 on phyb.
35 BRI1 and BAK1 are Phosphorylated at Many Sites unknown What are the function(s) in vivo? P -Tyr-831 Expression of sitedirected Tyr mutants in transgenic plants P -Tyr-610
36 고등식물의 LRR-RLKs 연구현황 Arabidopsis thaliana : 250 Leucine-Rich Repeat Receptor-Like Kinases (LRR-RLKs) Oryza sativa : 1,200 LRR-RLKs Brassica rapa : 300 LRR-RLKs BRI1 BAK1 FER cell elongation, growth, yield SAM maintenance CLV1 BAM1/2 abiotic stress response RPK1 PERK4 CRK36 floral abscission HAE HSL2 ERECTA ERL1 ERL2 stomatal development plant innate immunity FLS2 EFR PEPR1/2 BAK1 Xa21(rice) 36
37 세포막수용체인산화신호전달경로의중요성 ERECTA: 기공발달 BRI1: 세포신장촉진식물의생장과발달에중요 Biotic/abiotic 스트레스저항성작물의수확량증대 FLS2: 병저항성 37
38 Overview on flowering pathways in Arabidopsis FLC and other FLC-related proteins repress floral integrator genes, including FT, FD and SOC1, in Arabidopsis. Upon the activation of floral integrators, the floral transition ensues. FT is induced by the photoperiod pathway through the activation of CO. FT protein is a mobile flowering signal that physically interacts with FD protein at meristem to activate SOC1 and other floral activators. Therefore, FLC and CO antagonistically determine proper timing of flowering in Arabidopsis. Two genetically independent pathways, vernalization and autonomous pathways, repress the transcription of FLC. The autonomous pathway is required for repression of FLC regardless of environment stimuli. The vernalization pathway triggers stable repression of FLC. Gibberellin, a phytohormone, independently promotes flowering through the activation of SOC1 and other floral activator genes.
39 Vernalization-mediated acceleration of flowering Winter-annual strains of Arabidopsis flower late without vernalization (Left). Flowering of winter-annual strains of Arabidopsis is accelerated by vernalization (Right)
40 Cooperative activity of VIN3 and PRC2 for the repression of FLC by vernalization. PRC2 mediates tri-methylation of H3K27 at FLC chromatin. H3K9me2 at FLC chromatin can be recognized by VIN3 and VIL1/VRN5 through their PHD motifs. VIN3 and VIL1/VRN5 physically associate with PRC2 and enhance the H3K27 methylation activity of PRC2.
41 Schematic representation of mechanisms underlying FLC activation and repression A) Prior to vernalization (fall), FLC is highly expressed by activation chromatin-remodeling complexes, PAF1-C, COMPASS-C and RAD6-BRE1-C. B) During winter, a long ncrna, COLDAIR, is transcribed from the first intron of FLC and functions to recruit PRC2. COOLAIR and VIN3 is also transiently induced by cold and PRC2 together with PHD finger proteins, VIN3 and VIL1/VRN5, becomes associated with FLC chromatin. Level of FLC mrna decreases during cold exposure. C) After cold (Spring), the repressed state of FLC is stably maintained through combinatorial activities of PRC2 and PRC1-like complex.
42 Models of flowering time regulation by vernalization in various flowering plants Green: floral activator, Pink: floral repressor, Violet: upstream repressor of floral repressor.
43 FLC-promoted germination involves the ABA catabolic pathway (via CYP707A2) and GA biosynthetic pathway (via GA20ox1) in seeds. (A) Proportion of viable seed germination (±1 SE). C, control; U, uniconazol; F, flouridone; U+F, uniconazol + flouridone. Asterisks indicate significant differences between WT and their respective NIL or 35S::FLC overexpressor. (B) The expression (±1 SE) of CYP707A2 in NIL-FLCCvi and Ler seeds at different stages. (C) Expression of GA20ox1 (±1 SE) at different stages. (D) Simplified pathway model of the hypothesized connections between flowering and germination pathways, and the possible signal transduction during flowering (Left) and germination (Right). AP1 repression by high FLC expression during seed development directly or indirectly influences CYP707A2 and GA20ox1 through unknown pathways in germinating seeds. Chiang et al., (2009) PNAS 106:
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