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Plant Physiology Oct 2021Photosensory adaptation, which can be classified as sensor or effector adaptation, optimizes the light sensing of living organisms by tuning their sensitivity to...
Photosensory adaptation, which can be classified as sensor or effector adaptation, optimizes the light sensing of living organisms by tuning their sensitivity to changing light conditions. During the phototropic response in Arabidopsis (Arabidopsis thaliana), the light-dependent expression controls of blue-light (BL) photoreceptor phototropin 1 (phot1) and its modulator ROOT PHOTOTROPISM2 (RPT2) are known as the molecular mechanisms underlying sensor adaptation. However, little is known about effector adaption in plant phototropism. Here, we show that control of the phosphorylation status of NONPHOTOTROPIC HYPOCOTYL3 (NPH3) leads to effector adaptation in hypocotyl phototropism. We generated unphosphorable and phosphomimetic NPH3 proteins on seven phosphorylation sites in the etiolated seedlings of Arabidopsis. Unphosphorable NPH3 showed a shortening of its retention time in the cytosol and caused an inability to adapt to very low fluence rates of BL (∼10-5 µmol m-2 s-1) during the phototropic response. In contrast, the phosphomimetic NPH3 proteins had a lengthened retention time in the cytosol and could not enable the adaptation to BL at fluence rates of 10-3 µmol m-2 s-1 or more. Our results indicate that the activation level of phot1 and the corresponding phosphorylation level of NPH3 determine the dissociation rate and the reassociation rate of NPH3 on the plasma membrane, respectively. These mechanisms may moderately maintain the active state of phot1 signaling across a broad range of BL intensities and contribute to the photosensory adaptation of phot1 signaling during the phototropic response in hypocotyls.
Topics: Arabidopsis; Phosphorylation; Phototropism; Signal Transduction
PubMed: 34608954
DOI: 10.1093/plphys/kiab281 -
Scientific Reports Sep 2021Flavocoenzymes are nearly ubiquitous cofactors that are involved in the catalysis and regulation of a wide range of biological processes including some light-induced...
Flavocoenzymes are nearly ubiquitous cofactors that are involved in the catalysis and regulation of a wide range of biological processes including some light-induced ones, such as the photolyase-mediated DNA repair, magnetoreception of migratory birds, and the blue-light driven phototropism in plants. One of the factors that enable versatile flavin-coenzyme biochemistry and biophysics is the fine-tuning of the cofactor's frontier orbital by interactions with the protein environment. Probing the singly-occupied molecular orbital (SOMO) of the intermediate radical state of flavins is therefore a prerequisite for a thorough understanding of the diverse functions of the flavoprotein family. This may be ultimately achieved by unravelling the hyperfine structure of a flavin by electron paramagnetic resonance. In this contribution we present a rigorous approach to obtaining a hyperfine map of the flavin's chromophoric 7,8-dimethyl isoalloxazine unit at an as yet unprecedented level of resolution and accuracy. We combine powerful high-microwave-frequency/high-magnetic-field electron-nuclear double resonance (ENDOR) with C isotopologue editing as well as spectral simulations and density functional theory calculations to measure and analyse C hyperfine couplings of the flavin cofactor in DNA photolyase. Our data will provide the basis for electronic structure considerations for a number of flavin radical intermediates occurring in blue-light photoreceptor proteins.
PubMed: 34521887
DOI: 10.1038/s41598-021-97588-7 -
Proceedings of the National Academy of... Jan 2023Plants have developed intricate mechanisms to adapt to changing light conditions. Besides phototropism and heliotropism (differential growth toward light and diurnal...
Plants have developed intricate mechanisms to adapt to changing light conditions. Besides phototropism and heliotropism (differential growth toward light and diurnal motion with respect to sunlight, respectively), chloroplast motion acts as a fast mechanism to change the intracellular structure of leaf cells. While chloroplasts move toward the sides of the plant cell to avoid strong light, they accumulate and spread out into a layer on the bottom of the cell at low light to increase the light absorption efficiency. Although the motion of chloroplasts has been studied for over a century, the collective organelle motion leading to light-adapting self-organized structures remains elusive. Here, we study the active motion of chloroplasts under dim-light conditions, leading to an accumulation in a densely packed quasi-2D layer. We observe burst-like rearrangements and show that these dynamics resemble systems close to the glass transition by tracking individual chloroplasts. Furthermore, we provide a minimal mathematical model to uncover relevant system parameters controlling the stability of the dense configuration of chloroplasts. Our study suggests that the meta-stable caging close to the glass transition in the chloroplast monolayer serves a physiological relevance: Chloroplasts remain in a spread-out configuration to increase the light uptake but can easily fluidize when the activity is increased to efficiently rearrange the structure toward an avoidance state. Our research opens questions about the role that dynamical phase transitions could play in self-organized intracellular responses of plant cells toward environmental cues.
Topics: Plant Cells; Chloroplasts; Sunlight; Phototropism; Plant Leaves; Light
PubMed: 36638210
DOI: 10.1073/pnas.2216497120 -
Stress Biology Jul 2023Phototropism is a classic adaptive growth response that helps plants to enhance light capture for photosynthesis. It was shown that hydrogen peroxide (HO) participates...
Phototropism is a classic adaptive growth response that helps plants to enhance light capture for photosynthesis. It was shown that hydrogen peroxide (HO) participates in the regulation of blue light-induced hypocotyl phototropism; however, the underlying mechanism is unclear. In this study, we demonstrate that the unilateral high-intensity blue light (HBL) could induce asymmetric distribution of HO in cotton hypocotyls. Disruption of the HBL-induced asymmetric distribution of HO by applying either HO itself evenly on the hypocotyls or HO scavengers on the lit side of hypocotyls could efficiently inhibit hypocotyl phototropic growth. Consistently, application of HO on the shaded and lit sides of the hypocotyls led to reduced and enhanced hypocotyl phototropism, respectively. Further, we show that HO inhibits hypocotyl elongation of cotton seedlings, thus supporting the repressive role of HO in HBL-induced hypocotyl phototropism. Moreover, our results show that HO interferes with HBL-induced asymmetric distribution of auxin in the cotton hypocotyls. Taken together, our study uncovers that HO changes the asymmetric accumulation of auxin and inhibits hypocotyl cell elongation, thus mediating HBL-induced hypocotyl phototropism.
PubMed: 37676397
DOI: 10.1007/s44154-023-00111-3 -
Frontiers in Microbiology 2022Bilins are open-chain tetrapyrroles synthesized in phototrophs by successive enzymic reactions catalyzed by heme oxygenases (HMOXs/HOs) and ferredoxin-dependent...
Bilins are open-chain tetrapyrroles synthesized in phototrophs by successive enzymic reactions catalyzed by heme oxygenases (HMOXs/HOs) and ferredoxin-dependent biliverdin reductases (FDBRs) that typically serve as chromophore cofactors for phytochromes and phycobiliproteins. lacks both phycobiliproteins and phytochromes. Nonetheless, the activity and stability of photosystem I (PSI) and the catalytic subunit of magnesium chelatase (MgCh) named CHLH1 are significantly reduced and phototropic growth is significantly attenuated in a mutant that is deficient in bilin biosynthesis. Consistent with these findings, previous studies on uncovered an essential role for bilins in chloroplast retrograde signaling, maintenance of a functional photosynthetic apparatus, and the direct regulation of chlorophyll biosynthesis. In this study, we generated and screened a collection of insertional mutants in a genetic background for suppressor mutants with phototropic growth restored to rates observed in wild-type 4A+ cells. Here, we characterized a suppressor of named with phototrophic growth rates and levels of CHLH1 and PSI proteins similar to 4A+. Tetrad analysis indicated that a plasmid insertion co-segregated with the suppressor phenotype of . Results from TAIL-PCR and plasmid rescue experiments demonstrated that the plasmid insertion was located in exon 1 of the locus. Heterologous expression of the bilin-binding reporter NpF2164g5 in the chloroplast of indicated that bilin accumulated in the chloroplast of despite the absence of the HMOX1 protein. Collectively, our study reveals the presence of an alternative bilin biosynthetic pathway independent of HMOX1 in the chloroplasts of Chlamydomonas cells.
PubMed: 36003942
DOI: 10.3389/fmicb.2022.956554 -
Proceedings of the National Academy of... Jul 2020Fossilized carotenoid hydrocarbons provide a window into the physiology and biochemistry of ancient microbial phototrophic communities for which only a sparse and...
Fossilized carotenoid hydrocarbons provide a window into the physiology and biochemistry of ancient microbial phototrophic communities for which only a sparse and incomplete fossil record exists. However, accurate interpretation of carotenoid-derived biomarkers requires detailed knowledge of the carotenoid inventories of contemporary phototrophs and their physiologies. Here we report two distinct patterns of fossilized C diaromatic carotenoids. Phanerozoic marine settings show distributions of diaromatic hydrocarbons dominated by isorenieratane, a biomarker derived from low-light-adapted phototrophic green sulfur bacteria. In contrast, isorenieratane is only a minor constituent within Neoproterozoic marine sediments and Phanerozoic lacustrine paleoenvironments, for which the major compounds detected are renierapurpurane and renieratane, together with some novel C and C carotenoid degradation products. This latter pattern can be traced to cyanobacteria as shown by analyses of cultured taxa and laboratory simulations of sedimentary diagenesis. The cyanobacterial carotenoid synechoxanthin, and its immediate biosynthetic precursors, contain thermally labile, aromatic carboxylic-acid functional groups, which upon hydrogenation and mild heating yield mixtures of products that closely resemble those found in the Proterozoic fossil record. The Neoproterozoic-Phanerozoic transition in fossil carotenoid patterns likely reflects a step change in the surface sulfur inventory that afforded opportunities for the expansion of phototropic sulfur bacteria in marine ecosystems. Furthermore, this expansion might have also coincided with a major change in physiology. One possibility is that the green sulfur bacteria developed the capacity to oxidize sulfide fully to sulfate, an innovation which would have significantly increased their capacity for photosynthetic carbon fixation.
Topics: Carotenoids; Chromatography, Liquid; Cyanobacteria; Gas Chromatography-Mass Spectrometry; Mass Spectrometry; Photosynthesis; Pigments, Biological; Sulfur
PubMed: 32647063
DOI: 10.1073/pnas.2006379117 -
The Plant Cell Jun 2023PHYTOCHROME KINASE SUBSTRATE (PKS) proteins are involved in light-modulated changes in growth orientation. They act downstream of phytochromes to control hypocotyl...
PHYTOCHROME KINASE SUBSTRATE (PKS) proteins are involved in light-modulated changes in growth orientation. They act downstream of phytochromes to control hypocotyl gravitropism in the light and act early in phototropin signaling. Despite their importance for plant development, little is known about their molecular mode of action, except that they belong to a protein complex comprising phototropins at the plasma membrane (PM). Identifying evolutionary conservation is one approach to revealing biologically important protein motifs. Here, we show that PKS sequences are restricted to seed plants and that these proteins share 6 motifs (A to F from the N to the C terminus). Motifs A and D are also present in BIG GRAIN, while the remaining 4 are specific to PKSs. We provide evidence that motif C is S-acylated on highly conserved cysteines, which mediates the association of PKS proteins with the PM. Motif C is also required for PKS4-mediated phototropism and light-regulated hypocotyl gravitropism. Finally, our data suggest that the mode of PKS4 association with the PM is important for its biological activity. Our work, therefore, identifies conserved cysteines contributing to PM association of PKS proteins and strongly suggests that this is their site of action to modulate environmentally regulated organ positioning.
Topics: Phytochrome; Arabidopsis Proteins; Arabidopsis; Protein S; Light; Phototropism; Hypocotyl; Acylation
PubMed: 36972404
DOI: 10.1093/plcell/koad096 -
Communications Biology Jan 2022Human cone phototropism is a key mechanism underlying the Stiles-Crawford effect, a psychophysiological phenomenon according to which photoreceptor outer/inner segments...
Human cone phototropism is a key mechanism underlying the Stiles-Crawford effect, a psychophysiological phenomenon according to which photoreceptor outer/inner segments are aligned along with the direction of incoming light. However, such photomechanical movements of photoreceptors remain elusive in mammals. We first show here that primate cone photoreceptors have a planar polarity organized radially around the optical center of the eye. This planar polarity, based on the structure of the cilium and calyceal processes, is highly reminiscent of the planar polarity of the hair cells and their kinocilium and stereocilia. Secondly, we observe under super-high resolution expansion microscopy the cytoskeleton and Usher proteins architecture in the photoreceptors, which appears to establish a mechanical continuity between the outer and inner segments. Taken together, these results suggest a comprehensive cellular mechanism consistent with an active phototropism of cones toward the optical center of the eye, and thus with the Stiles-Crawford effect.
Topics: Animals; Biomechanical Phenomena; Cell Polarity; Cytoskeleton; Light; Macaca fascicularis; Reproducibility of Results; Retinal Cone Photoreceptor Cells; Retinal Rod Photoreceptor Cells
PubMed: 35075261
DOI: 10.1038/s42003-021-02998-y -
Plants (Basel, Switzerland) Jan 2024Gravitropism is the plant organ bending in response to gravity. Gravitropism, phototropism and sufficient mechanical strength define the optimal position of young shoots...
Gravitropism is the plant organ bending in response to gravity. Gravitropism, phototropism and sufficient mechanical strength define the optimal position of young shoots for photosynthesis. Etiolated wild-type Arabidopsis seedlings grown horizontally in the presence of sucrose had a lot more upright hypocotyls than seedlings grown without sucrose. We studied the mechanism of this effect at the level of cell wall biomechanics and biochemistry. Sucrose strengthened the bases of hypocotyls and decreased the content of mannans in their cell walls. As sucrose is known to increase the gravitropic bending of hypocotyls, and mannans have recently been shown to interfere with this process, we examined if the effect of sucrose on shoot gravitropism could be partially mediated by mannans. We compared cell wall biomechanics and metabolomics of hypocotyls at the early steps of gravitropic bending in Col-0 plants grown with sucrose and mannan-deficient mutant seedlings. Sucrose and mannans affected gravitropic bending via different mechanisms. Sucrose exerted its effect through cell wall-loosening proteins, while mannans changed the walls' viscoelasticity. Our data highlight the complexity of shoot gravitropism control at the cell wall level.
PubMed: 38256762
DOI: 10.3390/plants13020209 -
The Plant Cell Sep 2019In the course of evolution, plants have developed mechanisms that orient their organs toward the incoming light. At the seedling stage, positive phototropism is mainly...
In the course of evolution, plants have developed mechanisms that orient their organs toward the incoming light. At the seedling stage, positive phototropism is mainly regulated by phototropin photoreceptors in blue and UV wavelengths. Contrasting with this, we report that UV RESISTANCE LOCUS8 (UVR8) serves as the predominant photoreceptor of UV-B-induced phototropic responses in Arabidopsis () inflorescence stems. We examined the molecular mechanisms underlying this response and our findings support the Blaauw theory (Blaauw, 1919), suggesting rapid differential growth through unilateral photomorphogenic growth inhibition. UVR8-dependent UV-B light perception occurs mainly in the epidermis and cortex, but deeper tissues such as endodermis can also contribute. Within stems, a spatial difference of UVR8 signal causes a transcript and protein increase of transcription factors ELONGATED HYPOCOTYL5 (HY5) and its homolog HY5 HOMOLOG at the UV-B-exposed side. The irradiated side shows (1) strong activation of flavonoid synthesis genes and flavonoid accumulation; (2) increased gibberellin (GA)2-oxidase expression, diminished GA1 levels, and accumulation of the DELLA protein REPRESSOR OF GA1; and (3) increased expression of the auxin transport regulator , contributing to diminished auxin signaling. Together, the data suggest a mechanism of phototropin-independent inflorescence phototropism through multiple, locally UVR8-regulated hormone pathways.
Topics: Arabidopsis; Arabidopsis Proteins; Basic-Leucine Zipper Transcription Factors; Chromosomal Proteins, Non-Histone; Flavonoids; Gene Expression Profiling; Gene Expression Regulation, Plant; Indoleacetic Acids; Inflorescence; Phototropism; Plant Stems; Protein Serine-Threonine Kinases; Signal Transduction; Ultraviolet Rays
PubMed: 31289115
DOI: 10.1105/tpc.18.00929