BackgroundPlants have evolved various sophisticated mechanisms to respond and adapt to changes of abiotic factors in their natural environment. Light is one of the most important abiotic environmental factors and it regulates plant growth and development throughout their entire life cycle. To monitor the intensity and spectral composition of the ambient light environment, plants have evolved multiple photoreceptors, including the red/far-red light-sensing phytochromes.Methodology/Principal FindingsWe have developed an integrative mathematical model that describes how phytochrome B (phyB), an essential receptor in Arabidopsis thaliana, controls growth. Our model is based on a multiscale approach and connects the mesoscopic intracellular phyB protein dynamics to the macroscopic growth phenotype. To establish reliable and relevant parameters for the model phyB regulated growth we measured: accumulation and degradation, dark reversion kinetics and the dynamic behavior of different nuclear phyB pools using in vivo spectroscopy, western blotting and Fluorescence Recovery After Photobleaching (FRAP) technique, respectively.Conclusions/SignificanceThe newly developed model predicts that the phyB-containing nuclear bodies (NBs) (i) serve as storage sites for phyB and (ii) control prolonged dark reversion kinetics as well as partial reversibility of phyB Pfr in extended darkness. The predictive power of this mathematical model is further validated by the fact that we are able to formalize a basic photobiological observation, namely that in light-grown seedlings hypocotyl length depends on the total amount of phyB. In addition, we demonstrate that our theoretical predictions are in excellent agreement with quantitative data concerning phyB levels and the corresponding hypocotyl lengths. Hence, we conclude that the integrative model suggested in this study captures the main features of phyB-mediated photomorphogenesis in Arabidopsis.
Plant photoreceptor phytochromes are phosphoproteins, but the question as to the functional role of phytochrome phosphorylation has remained to be elucidated. We investigated the functional role of phytochrome phosphorylation in plant light signaling using a Pfr-specific phosphorylation site mutant, Ser598Ala of oat (Avena sativa) phytochrome A (phyA). The transgenic Arabidopsis thaliana (phyA-201 background) plants with this mutant phyA showed hypersensitivity to light, suggesting that phytochrome phosphorylation at Serine-598 (Ser598) in the hinge region is involved in an inhibitory mechanism. The phosphorylation at Ser598 prevented its interaction with putative signal transducers, Nucleoside Diphosphate Kinase-2 and Phytochrome-Interacting Factor-3. These results suggest that phosphorylation in the hinge region of phytochromes serves as a signal-modulating site through the protein–protein interaction between phytochrome and its putative signal transducer proteins.
Phytochrome (phy) A mediates two distinct photobiological responses in plants: the very-low-fluence response (VLFR), which can be saturated by short pulses of very-low-fluence light, and the high-irradiance response (HIR), which requires prolonged irradiation with higher fluences of far-red light (FR). To investigate whether the VLFR and HIR involve different domains within the phyA molecule, transgenic tobacco (Nicotiana tabacum cv Xanthi) and Arabidopsis seedlings expressing full-length (FL) and various deletion mutants of oat (Avena sativa) phyA were examined for their light sensitivity. Although most mutants were either partially active or inactive, a strong differential effect was observed for the ⌬6-12 phyA mutant missing the serine-rich domain between amino acids 6 and 12. ⌬6-12 phyA was as active as FL phyA for the VLFR of hypocotyl growth and cotyledon unfolding in Arabidopsis, and was hyperactive in the VLFR of hypocotyl growth and cotyledon unfolding in tobacco, and the VLFR blocking subsequent greening under white light in Arabidopsis. In contrast, ⌬6-12 phyA showed a dominant-negative suppression of HIR in both species. In hypocotyl cells of Arabidopsis irradiated with FR phyA:green fluorescent protein (GFP) and ⌬6-12 phyA:GFP fusions localized to the nucleus and coalesced into foci. The proportion of nuclei with abundant foci was enhanced by continuous compared with hourly FR provided at equal total fluence in FL phyA:GFP, and by ⌬6-12 phyA mutation under hourly FR. We propose that the N-terminal serine-rich domain of phyA is involved in channeling downstream signaling via the VLFR or HIR pathways in different cellular contexts.Phytochromes (phy) comprise a family of photoreceptors that help adjust plant growth and development to the ambient light environment. These photoreceptors sense red light (R) and far-red light (FR) through photo-interconversion between two stable conformations, an R-absorbing Pr form and an FRabsorbing Pfr form. In seed plants such as Arabidopsis, as many as five phy isoforms are present (Mathews and Sharrock, 1997). One of the more influential is phyA, the most abundant isoform in darkgrown seedlings (Hirschfeld et al., 1998). phyA helps perceive (a) the brief light pulses that can promote seed germination (Botto et al., l996; Shinomura et al., 1996), (b) the difference between darkness and the FR-rich environment that initiates de-etiolation beneath dense canopies (Yanovsky et al., 1995), (c) the changes in irradiance associated with the presence of neighboring vegetation (Yanovsky et al., 1998), and (d) the duration of the photoperiod (Johnson et al., 1994).phyA can initiate two photobiologically distinct responses, the very-low-fluence responses (VLFRs) and the high-irradiance responses (HIRs). The VLFR can be achieved by short intermittent pulses of R or FR. For example, the VLFR that inhibits hypocotyl growth can be saturated in Arabidopsis by a 3-min pulse of FR every 2 h with the half-maximal effect requiring 0.1 mol m Ϫ2 s Ϫ1 of FR (Casal et al., 2000). In contra...
Summary The photoreceptor phytochrome A acts as a light‐dependent molecular switch and regulates responses initiated by very low fluences of light (VLFR) and high fluences (HIR) of far‐red light. PhyA is expressed ubiquitously, but how phyA signaling is orchestrated to regulate photomorphogenesis is poorly understood. To address this issue, we generated transgenic Arabidopsis thaliana phyA‐201 mutant lines expressing the biologically active phyA‐YFP photoreceptor in different tissues, and analyzed the expression of several reporter genes, including ProHY5:HY5‐GFP and Pro35S:CFP‐PIF1, and various FR‐HIR‐dependent physiological responses. We show that phyA action in one tissue is critical and sufficient to regulate flowering time and root growth; control of cotyledon and hypocotyl growth requires simultaneous phyA activity in different tissues; and changes detected in the expression of reporters are not restricted to phyA‐containing cells. We conclude that FR‐HIR‐controlled morphogenesis in Arabidopsis is mediated partly by tissue‐specific and partly by intercellular signaling initiated by phyA. Intercellular signaling is critical for many FR‐HIR induced responses, yet it appears that phyA modulates the abundance and activity of key regulatory transcription factors in a tissue‐autonomous fashion.
Background:Plants have evolved various sophisticated mechanisms to respond and adapt to changes of abiotic factors in their natural environment. Light is one of the most important abiotic environmental factors and it regulates plant growth and development throughout their entire life cycle. To monitor the intensity and spectral composition of the ambient light environment, plants have evolved multiple photoreceptors, including the red/far-red light-sensing phytochromes.Methodology/Principal Findings: We have developed an integrative mathematical model that describes how phytochrome B (phyB), an essential receptor in Arabidopsis thaliana, controls growth. Our model is based on a multiscale approach and connects the mesoscopic intracellular phyB protein dynamics to the macroscopic growth phenotype. To establish reliable and relevant parameters for the model phyB regulated growth we measured: accumulation and degradation, dark reversion kinetics and the dynamic behavior of different nuclear phyB pools using in vivo spectroscopy, western blotting and Fluorescence Recovery After Photobleaching (FRAP) technique, respectively.Conclusions/Significance: The newly developed model predicts that the phyB-containing nuclear bodies (NBs) (i) serve as storage sites for phyB and (ii) control prolonged dark reversion kinetics as well as partial reversibility of phyB Pfr in extended darkness. The predictive power of this mathematical model is further validated by the fact that we are able to formalize a basic photobiological observation, namely that in light-grown seedlings hypocotyl length depends on the total amount of phyB. In addition, we demonstrate that our theoretical predictions are in excellent agreement with quantitative data concerning phyB levels and the corresponding hypocotyl lengths. Hence, we conclude that the integrative model suggested in this study captures the main features of phyB-mediated photomorphogenesis in Arabidopsis.
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